Open access

Amygdala and Emotional Learning in Vertebrates – A Comparative Perspective

Written By

Juan Pedro Vargas, Juan Carlos López and Manuel Portavella

Submitted: 14 December 2011 Published: 19 December 2012

DOI: 10.5772/51552

From the Edited Volume

The Amygdala - A Discrete Multitasking Manager

Edited by Barbara Ferry

Chapter metrics overview

3,360 Chapter Downloads

View Full Metrics

6. 1. Introduction

The mammalian amygdala is a telencephalic structure of complex embryonic origin, composed of several nuclei that proceed from both the telencephalic pallial wall and the striated sheet, settling a border or transition zone between the telencephalic pallium and subpallium. In primates, the amygdala is located in the anterior temporal lobe, and in other mammals occupies a topologically equivalent position. Klüver & Bucy (1939) described a syndrome after bilateral ablation of the temporal lobes of rhesus monkeys which, among other symptoms, caused a dramatic decrease in the emotional reaction of fear, an effect attributed primarily to the ablation of the amygdaline system rather than other structures. This effect sparked interest in studying the possible involvement of the amygdala in emotional responses, such as learning and emotional memory that has been developed since the second half of the 20th century. In fact, bilateral lesions to the amygdala (or its equivalent anatomical structure) in other vertebrate groups (reptiles, birds, and non-primate mammals) cause serious interference with the normal development of emotional responses characteristic of the species such as aggressive, sexual, or parental behavior (Kling & Brothers, 1992). Studies about emotional and avoidance (active or passive) conditioning show that the complete or partial injury to amygdala causes serious disorders in these learned responses (LeDoux, 1995). Moreover, the amygdala is involved in memory and attention processes (Kapp et al., 1992), in the emotional evaluation of stimuli (Davis, 1992; Gallagher & Chiba, 1996; Gallagher & Holland, 1992; Halgren, 1992; LeDoux, 1992, 1995) and in emotional aspects of dreams (Calvo et al., 1987). In the past, its intricate structure and the paradoxical experimental results that sometimes were obtained in both humans and animals (Phelps & Anderson, 1997) have been especially confusing when trying to clearly identify its functions. Although, a common factor found in these data is its emotional aspect. It has now become clear that it is also involved in humans’ social learning of fear and in anxiety disorders (Olsson & Phelps, 2007). In fact, it appears that stimuli that are not consciously perceived activate the amygdala; this provides a fast and automatic processing of the stimuli for social cognition (Adolphs, 2009), especially with regard to facial expression (Adolphs et al., 1994).

As stated above, the amygdala is not a uniform structure, not only in terms of the structural differences but also by the intrinsic and extrinsic pattern of afferents and efferents of its different nuclei, including the divisions of the subnuclei (Amaral et al., 1992; Pitkänen et al., 1997), which also appears to be involved in different functions for different circuits. Lesion and stimulation studies may lead to varying results depending on the affected circuit, but always shows implicit emotional factors (Davis, 1992; Gallagher & Chiba, 1996; Gallagher & Holland, 1992; Killcross et al., 1997; LeDoux, 1992). In the human case, the amygdala could be considered an essential part of the brain involved in surveillance tasks of potentially ambiguous or unpredictable stimuli (Whalen, 1999).

Figure 1.

Phylogeny of vertebrates represented in a cladogram. Although the first fossil records are from the Ordovician period, the existence of vertebrates in the Cambrian is very likely. Fishlike vertebrates gave rise to the agnatha (jawless fish) and gnathostomes (jawed fish). The current vertebrates descended from one of these two groups. Gnathostomes were diversified into different classes, such as reptilians, birds, and mammals. Current bony fishes present brain structures with a cytoarchitecture and function very close to the amygdala in mammals. This data indicates that most likely a common ancestor to vertebrates had a brain with a structure functionally similar to the amygdala, and because of its adaptive value, it was conserved throughout the phylogeny.

It is considered that the amygdala is not an exclusive structure of mammals, since genoarchitectonic, neurochemical, embryological, anatomical, and behavioral studies in a comparative perspective (Aggleton, 1992; Bruce & Neary, 1995; Macphail, 1996; Medina et al., 2011; Moreno & González, 2006; 2007; Parent, 1986; Sriedter, 1997; Wulliman & Rink, 2002) have proposed several homologies for this structure in other vertebrate groups (fish, amphibians, reptiles, and birds). Although there has been no complete agreement on the homology of all parts of this structure (pallial and subpallial portion) among all vertebrate groups over time (Braford, 1995; Bruce & Neary, 1995; Northcutt, 1995; Sriedter, 1997), the existence of a basic scheme of the amygdala in fish, reptiles, birds, and mammals, irrespective of the diverse differentiation of this structure along the evolution of the different groups of tetrapods has been established by examining the comparative genoarchitecture (Medina et al., 2011; Moreno & González, 2006; 2007). In this sense, it is possible that the amygdala or analogous structure was present in an ancestor of current vertebrates. Its function was necessary for the adaptative processes, and it was conserved along the vertebrate radiation (figure 1).


2. The amygdala. Homologies among vertebrates

As noted previously, the amygdala of mammals and other tetrapods is divided into two main parts, one pallial or cortical, and another subpallial or striated. In addition, it is divided into different nuclei, and these divisions also seem to be found in groups other than mammals, such as reptiles and birds (Bruce & Neary, 1995; DeOlmos et al, 1985; Lohman & Smeets, 1990; McDonald, 1992; Medina et al., 2011; Moreno & González, 2007; Northcutt, 2008; Striedter, 1997; Wulliman & Rink, 2002; Zeier & Karten, 1971). In the case of chondrichthyan fish the so-called Nucleus A is recognized as a possible homologue of the tetrapod pallial amygdala, both for its position and its pattern of connectivity (Northcutt, 1995; 2008; Smeets, 1990). In actinopterygians, the telencephalon undergoes an eversion process that raises a serious difficulty in establishing homologies with the amygdala (Braford, 1995; Gage, 1983; Scalia & Ebbesson, 1971). However, the cytoarchitecture, the neurohistochemistry, studies of embryonic development, the pattern of connectivity and topological studies (Braford, 1995; Chanconie & Clairambault, 1975; Morgan, 1974a, 1974b; Murakami et al., 1983; Northcutt, 1981; 1995; Northcutt & Braford, 1980) suggest that the region Dmv of the teleost telencephalon is a good candidate to be considered the homologue of the pallial amygdala (Northcutt, 1995; Northcutt & Braford, 1980), although other authors suggest that Dmv could be homologous to the basal ganglia or the hippocampus of mammals (Murakami et al., 1983; Parent et al., 1978). Moreover, the pattern of connectivity, with strong sensory thalamic inputs and reciprocal connections with the hypothalamus, gives a distinctly limbic character to Dmv (Braford, 1995; Echteler & Saidel, 1981; Ito et al., 1986; Murakami et al, 1983; Striedter, 1991). Another circumstance that would support the homology of Dmv with the pallial amygdala is its topological situation. The Dmv telencephalon is located between the ventral subpallial area (possible striated region) and the dorsoposterior area (main olfactory receptor area), a similar position to the pallial amygdala of other vertebrates, between the olfactory cortex and the subpallial amygdala (Braford, 1995; Bruce & Neary, 1995; Neary, 1990; Neary & Bruce, 1993; Northcutt & Kicliter, 1980). Other authors (Kyle & Peter, 1982; Kyle et al., 1982) have pointed to the region Vs-pVv (ventral area supracomisural ventral-ventral area) as homologous to the corticomedial amygdala, based on the fact that it receives olfactory afferents (Oka, 1980), the concentration of steroid hormone receptors (Kim et al., 1978; see Medina et al., 2011 for a review of steroid hormone-regulated as a component of the amygdala), and the results of electrolytic lesions (Kyle et al., 1982). This data is also supported by functional data as damage to this structure affects the male reproductive behavior and other signs of social interest such as parental care or aggressive behavior, the same pattern of deficits that is found with lesions of the corticomedial amygdala in mammals (Isaacson, 1976; Kling & Brothers, 1992). In fact, it has been proposed that the most medial region of the ventral area of the telencephalon in teleosts fish correspond to the subpallial amygdala (Northcutt, 1995; 2008; Northcutt & Braford, 1980).


3. Functions of the amygdala in emotional learning and memory in mammals

3.1. Amygdala and fear conditioning

The conditioning of the fear response in short delay procedures is affected by the lesion of specific areas of the amygdala, mainly the central, basal, and lateral nucleus (Davis, 1992; LeDoux, 1992; 1995). This conditioned fear response is established very easily and this characteristic seems to be preserved through evolution in all vertebrate groups (LeDoux 1992; Portavella et al, 2004a), and consists of three components: behavioral (eg usually appears a "freezing" response), autonomic (eg bradycardia response) and hormonal (eg increased levels of ACTH) (Davis, 1992). In the human case, the involvement of the amygdala in fear conditioning has been shown by both consciously and unconsciously processed stimuli (Morris et al., 1989). Thus, the lesion of the amygdala produces a serious effect on the ability to recognize expressions of fear (Adolphs et al., 1994; 2005), and thus interferes seriously in the early detection of emotional stimuli. Recent studies using functional imaging techniques have analyzed the role of different parts of the human limbic system in the processing of emotional discrimination of faces and natural scenes (Fusar-Poli et al., 2009; Sabatini et al., 2011)

To better understand the role of the amygdala in fear conditioning, it is necessary to know how the main efferents and afferents of the amygdalar structures are organized and their intrinsic connections (Amaral et al., 1992; Pitkänen et al., 1995; Pitkänen et al., 1997; Savander et al., 1995). In fact, the study of the function and the connectivity go hand in hand, since not all lesions nor interventions have the same effects in different amygdaloid nuclei; although some pallial nuclei (lateral, basal and accessory basal nuclei) and subpallial (central nucleus) appear to be more decisive in this type of conditioning (see LeDoux, 2000 for a review). In mammals, the lateral nucleus receives direct thalamic afferents from different sensory modalities (eg intralaminar nuclei, supregeniculate nucleus and medial division of the medial geniculate nucleus), so it receives somesthetic, visual, and auditory thalamic afferents (Campeau & Davis, 1995; Gallagher & Chiba, 1996; Rogan & LeDoux, 1995). The lesion of this nucleus produces a severe deficit in the expression of conditioned fear response, and also an inability to learn it (see Rosen, 2004). Also specific neurotoxic lesions in the basolateral complex (lateral and basal nuclei) prevent the animal from acquiring a conditioned fear response (Campeau & Davis, 1995; Rabinak & Maren, 2008). Inputs from cortical regions to the lateral nucleus send processed information of the same stimuli (sensory, association, and polymodal cortex), through a thalamo-cortico-amygdala via (for a review see Sah et al., 2003). The importance of the thalamus-amygdala via is proven by the fact that ablation or disconnection of sensory cortical region does not prevent fear conditioning to a single sound stimulus (DiChara et al., 1970; LeDoux et al., 1986). However, when the set of stimuli is more complex (such as in a program of differential conditioning where there are two different sounds as stimuli or a reinforced conditioned stimulus (CS +) and a non-reinforced one (CS-), and the animal during the training and reversal has to learn which one is paired with the EI (electric footshock), the lesion to this circuit disrupts the performance on this type of differential learning tasks (Jarrell et al., 1987). It has also been shown that the context can become a fundamental cue for learning. This contextual conditioning has been established when for example, the fear response occurs without the presence of the CS or the US (unconditioned stimulus), by merely placing an animal in the box in which it has been receiving these two paired stimuli. In this case, the presence of certain structures such as the hippocampus and related structures is essential, because the lesion of this structure is sufficient to block the fear response to the context (Nadel, 2008; Phillips &LeDoux, 1992; Selden et al., 1991; Wiltgen et al., 2006). Lesions of retrosplenial cortex (Keene & Bucci, 2008) and of the entorhinal cortex (Ji & Maren, 2008) also disrupt contextual fear conditioning. The entorhinal cortex is implicated in processing background contextual information given that NMDA lesions impair the processing of contextual background fear conditioning but not the fear conditioned to an auditory stimulus (Majchrzak et al., 2006). The hippocampus maintains connections to the lateral and basal nucleus via subiculum and with the basal nuclei (Ottersen, 1982). In this sense, the mere disconnection of this afferent or lesion to the hippocampus is enough to prevent and suppress emotional conditioning context (Maren & Fanselow, 1995; Phillips &LeDoux, 1992). All available data point to the lateral nucleus as a nucleus of sensory input to the amygdala (Rogan & LeDoux, 1995), which according to LeDoux (1995) could act as an interface and a major site for integration of information from the different inputs of sensory information during the conditioning of the fear response. The afferents of the lateral nucleus are directed to other amygdalar structures including the pallial basal and basal accessory nuclei too (Pitkänen & Amaral, 1991).

The basal nucleus (basal and basal accessory) receives input from the hippocampus and cortical association areas such as inferotemporal cortex and other structures (Amaral et al., 1992), and sends efferents to the sensory association cortex and the central nucleus (Aggleton, 1985; Amaral et al., 1992; Price & Amaral, 1981). Electrolytic or NMDA-induced lesion of the basolateral complex of the amygdala blocked fear conditioning to both visual and auditory CSs (Campeau & Davis, 1995). The use of substances that produce temporal inactivation such as muscimol (a GABA type A agonist) has introduced some controversy, since some studies show that injecting this substance in the basal and lateral nuclei produced different results depending on the time of injection. If the drug is injected before conditioning it results in acquisition deficits, although the same manipulation made immediately after conditioning has no effect (Helmstetter & Bellgowan, 1994). Nevertheless, with a similar design Muller et al. (1997) showed that injecting muscimol to functionally inactivate the basal or the lateral nucleus produced little conditioned fear to contextual or auditory conditioned stimuli. Herry et al. (2008) and Amano et al. (2010) have also shown that inactivation of the basal nuclei with muscimol does not block the expression of the conditioned fear. Fanselow & Kim (1994) did the same with the local infusion of d-APV (a NMDA receptor antagonist), obtaining similar results. Cousens & Otto (1998) analyzed the relation between the fear response to olfactory and contextual stimuli. The results showed that excitotoxic lesions (infusion of high concentration of NMDA) disrupted the conditioned response to odor and context. All the data supports the involvement of the amygdala in the acquisition of a conditioned fear response, such as in its expression, once conditioning is established.

The central nucleus, in contrast, has essentially extra-amygdala efferents, and maintains important connectivity with brainstem nuclei and areas, such as the periaqueductal gray matter, and lateral hypothalamus (Davis, 1992), which in turn control the response patterns that involve the emotional response of fear. In fact, the neurotoxic lesion of this structure impairs the learning of a conditioned fear response (Campeau & Davis, 1995).

3.2. Plasticity in the amygdala and fear conditioning

In rats, the plastic processes that take place in amygdala structures during learning of fear conditioning have been studied on the presence of postsynaptic long-term potentiation (Clugnet et al., 1990; Sah et al., 2008). Some of these studies found that these processes were not mediated by NMDA receptors (Chapman & Bellavance, 1992), as occurs in the hippocampus (Bliss & Collingridge, 1993; Hicks, 1995; Lynch et al., 1991; Madison et al., 1991; Malenka & Nicholl, 1993; McEntee & Crook, 1993; Morris et al, 1989; Witkin, 1995). Nevertheless, later studies found the existence of long-term potentiation processes mediated by NMDA receptors located in the lateral amygdala (Gean et al., 1993). Furthermore, these receptors located in the lateral amygdala are implicated in the processing of the conditioned stimulus in fear conditioning (Farb & LeDoux, 1997; Li et al., 1996). The use of antagonists of these receptors causes serious interference in the conditioning of the fear response to simple stimuli as the context, but not retention or expression of a learned response (Fanselow & Kim, 1994; Gerwirtz & Davis, 1997; Maren et al., 1996). “In vivo” and “in vitro” studies show how fear conditioning induces a process of long-term potentiation (LTP) mediated by NMDA receptors (Rogan et al., 1997; McKernan & Shinnick-Gallagher, 1997). It has also been shown that NMDA receptor blockade interferes with the process of extinction of a conditioned fear response (Falls et al., 1992). These results and their relationship to learning processes are parallel to those found in the hippocampus, and indicate that a long-term depression (LTD) also mediated by NMDA receptors, which has been linked to the extinction of responses acquired in other structures like the hippocampus, takes place in the amygdala too (Dudek & Bear, 1992). In fact, it has been proposed (LeDoux, 1995), that the convergence of sensory information of the conditioned and the unconditioned stimuli in the amygdala would follow Hebbian patterns (Hebb, 1949) and it would affect other areas involved in the process of emotional conditioning. In the last 20 years, a great amount of evidence (Johansen et al., 2011) showed that two kinds of molecular mechanisms are responsible for fear conditioning in the amygdala, specifically in the lateral amygdala: hebbian plasticity and neuromodulatory processes. In this sense, studies of fear conditioning to auditory stimuli suggest the existence of response potentiation in the lateral nucleus after learning. In addition, these plastic changes have also been observed in the auditory cortex. This change would be mediated by the circuit thalamus - lateral nucleus – basal nucleus - central nucleus - nucleus basalis of Meynert, since this latest nucleus sends a strong cholinergic innervation to the cerebral cortex (Price & Amaral, 1981; Russchen et al., 1985). It is very probable that this circuit has a key role in producing fast brain activity rhythms of low voltage (Bukasi et al., 1988). These results has been verified in studies that analyzed the involvement of the central nucleus of the amygdala in brain activation (Kapp et al, 1984; 1990; 1992) showing that activation of the amygdala and the prosencephalic basal nucleus produced cerebral asynchrony mediated by this cholinergic innervation. Therefore, the neuromodulatory processes in the glutamate amygdalar circuits (Ferry & McGaugh, 2008; Johansen et al., 2011) are mediated by monoamine transmitters (adrenaline, norepinephrine, and dopamine). The consolidation of this learning is dependent on plastic changes of amygdala synapses. The synthesis of a broad amount of proteins underlies consolidation of fear conditioning, such as receptor glutamate subunits, calmodulin, protein-kinases, and signaling pathway (see Helmstetter et al., 2008).

Experimental results show that the specific lesion of a thalamic region (that sends its efferents to the amygdala as the medial division of medial geniculate nucleus) can prevent the animal to be conditioned to a stimulus of that sensory modality (auditory), but not to another of different modality, such as visual (Campeau & Davis, 1995). On the other hand, different results show that the thalamo-amygdala and the thalamo-cortico-amygdala pathways are equipotential with the facilitation of classical conditioning to a simple stimulus (Johansen et al., 2011). These data indicate that there may be multiple and multi-modal representation of the CS-US associations in the amygdalar structure and the intrinsic circuits for fear conditioning (Gallagher & Chiba, 1996; LeDoux, 1995).

The neural system proposed by several authors for fear conditioning (Davis, 1992; LeDoux, 1995; Pitkänen et al, 1997) gives a central role to the amygdala as a receiving center of different information about stimuli, such as features of the stimuli (thalamus-lateral nucleus), perceptual phenomena (sensory association areas-lateral nucleus), spatial location and/or contextual and explicit memory (hippocampus-parvocellular division of the basal and lateral nucleus), polymodal representations (polymodal association cortex-lateral nucleus), and proprioceptive information (hypothalamus-medial nucleus). In this way, the response elicited by the circuit through the central nucleus would be induced by multiple representations of the existing stimulus in various structures, including the amygdala (Johansen et al., 2011).

3.3. Amygdala and avoidance conditioning

The studies on the involvement of the amygdala in avoidance learning performed between the decades of the 50’s and the 70’s were somewhat confusing (Brady et al., 1954; Campenot, 1969; Caruthers, 1969; Fonberg, 1973; Grossman, 1972; Grossman et al., 1974;, Isaacson, 1976; Kaada, 1972; Kling et al., 1960; McGaugh & Gold, 1976; Pellegrino, 1968; Ursin, 1965). After a critical reading of these works many of the lesions performed in the different studies affect more than one area, the procedures were not exactly comparable to one another, and it was unclear what the animals were really learning and in what context. However, while some results appear contradictory, it seems that it can be establish the differential involvement of some of the amygdaloid nuclei in the different types of avoidance behavior: passive, discriminative active -lever press- or one-way and two-way active discrimination (Ambrogli et al., 1991; Fonberg, 1973; Grossman et al., 1974; Handwerker et al., 1974; Horvath, 1963; Killcross et al., 1997; Liang & McGaugh, 1983; McIntery & Stein, 1973; Roozendaal et al., 1997; Sanchez-Riolobos 1986; van-der-Zee et al., 1997; Werka et al., 1978; Wiersma et al., 1998). The contradictory results mentioned above could be due to the fact that the amygdala has been considered a functional structure instead of a set of functional subsystems. The most important issues to consider when interpreting the different results on different types of avoidance behaviors are the result of overtraining, and hence the degree of consolidation of learning, individual differences (high-level avoidance animals and low-level avoidance animals within the same strain of animals), and of course, the verification of experimental procedures.

In addition, the similarity of lesions between different species, and defining which structures are affected are important data to analyze, since it has been shown that all these factors can dramatically influence the effects on acquisition or retention of this learned avoidance responses on apparently similar procedures as is exposed below.

3.4. Amygdala and olfactory conditioning

Fear conditioning studies have been directed primarily to analyzing the relationship between visual/auditory cues and the US, with little attention to olfactory cues. Studies with these types of cues are relatively recent although olfactory cues are of great evolutionary importance for laboratory animals such as rats. As with visual and auditory cues, studies that have used odors as CS associated with a foot-shock have recorded a strong emotional response, showing even greater resistance to extinction processes (Richardson et al. 2002). Electrophysiological studies also showed that the synaptic modifications in the BLA are dependent on the contingency between CS and US (Rosenkranz & Grace, 2002). Furthermore, this plasticity is also dependent of NMDA receptors during the acquisition process and is dependent of AMPA during recovery (Walker et al. 2005).

In addition to the BLA, other areas like the mPFC, perirhinal cortex and hippocampus specifically influence the expression of activity of the amygdala during fear conditioning odor. While the perirhinal cortex is essential for the initial processing of odor stimulus (Herzog & Otto, 1998), CA1 and CA3 of the hippocampus have been linked to the encoding and retrieval of context information (Hunsaker & Kesner, 2008). The subiculum is the principal structure linking the hippocampus with the entorhinal cortex and many other cortical and subcortical areas. Specifically, the v-Sub may act as an interface between the hippocampus as a contextual information processor and cortical and subcortical processing systems related to motivation such as the ventral striatum and amygdala (Floresco et al., 2001; Quintero et al, 2011; Traverso et al, 2010). Parsons & Otto (2008) showed that the inactivation of dorsal hippocampus using an olfactory contextual conditioning, caused acquisition and retrieval deficits. In addition, neurons from mPFC are essential to acquire the association between CS and UC. These neurons show strong activity to foot-shock odor association. This activity is dopamine dependent, given that selective blockade of dopamine receptors reduces emotional response to the CS (Laviolette et al. 2005).

3.5. Effects of lesions to the amygdala

Kaada (1972) postulated that there were two different regions in the amygdala for the control of active avoidance behavior in rats, the defense amygdalar region, and the basolateral complex. Partial or total lesion to the defense amygdalar region (in rats and cats including the ventral part of the internal capsule and the ventral amigdalofugal pathway and pallial and subpallian structures), suppressed defense responses including the escape response (Blanchard & Blanchard, 1972; Kemble et al., 1984; 1990; Ursin et al., 1981). So, in their view it would have to block active avoidance responses in a classical active avoidance response paradigm. In contrast, lesion to the basolateral complex, which had inhibitory influences, impairs passive avoidance behavior but it does not affect the performance in an active avoidance paradigm behavior. Several experimental results support this view: in cats, both the electrolytically lesion of the anterior portion of the lateral nucleus and the interruption of the amigdalofugal ventral pathway produced a severe deficit in active avoidance conditioning, but not in passive avoidance (Ursin, 1965). Also, electrolytic lesion to the central nucleus and to the adjacent and dorsal regions to the basolateral complex in cats affected the retention of a two-way active avoidance response, but it did not affect one way active avoidance nor passive avoidance (Horvath, 1963). Similar data were obtained in rats (Pellegrino 1968). In this study, a lesion to the basolateral complex produced a severe disability for the maintenance of a passive avoidance response. Also, in mice, a large electrolytic lesion produces a severe deficit in both active and passive avoidance responses (Takashina et al., 1995). According to Werka et al. (1978) a lesion to the lateral cortex and central and lateral nuclei described deficits in the retention of one-way active avoidance. Killcross et al. (1997) demonstrated a process that allowed them to separate two responses related to fear conditioning (a conditioned suppression response to an aversive stimulus and an active avoidance response to the harmful stimulus) that lesions to the central nucleus affect the maintenance of the conditioned suppression response, but not the acquisition of the active avoidance response. In contrast, lesions to the basolateral nucleus produced the opposite effect. This latest result would establish a parallel processing of two types of fear dependent response, indicating that in the amygdala there are different mechanisms and different areas for processing the stimuli and the fear response. This idea would lead to a more critical discussion about the nature of avoidance responses, but what concerns us is that the amygdala is establishing an important relationship with this type of learning. Other studies present conflicting results, for instance Brady et al. (1954), showed that a large electrolytic lesion to the amygdala impairs cats to acquire an active avoidance response, but if the lesion was done after the learning, it did not affect the maintenance of the response. Similar results were obtained with passive avoidance procedure after bilateral electrolytic lesions (Liang et al., 1982). Also, in rats the lesion to the central nucleus produced a deficit in the acquisition but not in the retention of the response (Davis, 2000; Grossman et al., 1974; McIntery & Stein, 1973). In addition, different molecular processes seem underlying to acquisition and retention in central amygdala. While the inhibitory consolidation processes are under control of NMDA and cannabinoid CB1 receptors (Ghiasvand et al., 2011), serotonergic system is involved in the modulation of retention in the passive-avoidance task (Schneider et al., 2003). Another set of results have raised deeper questions about the involvement of various amygdaloid nuclei, where the amygdaloid cortex lesion severely affected the acquisition of one and two-way active avoidance response. In contrast, lesions of the cortical, medial, central, intercalated, lateral, and basolateral nucleus did not affect active avoidance, although lesions to the central, intercalated, and basolateral nucleus impair passive avoidance learning (Grossman et al., 1974). A recent electrophysiological study shows that the expression of conditioned freezing depends on increased activity levels of the medial region of the central amygdala but it does not depend on the activity of the lateral region (Duvarci et al., 2011). These differences in results could be due to various reasons (e.g. lesion differences, collaterally affected areas, use of different strains, etc). Another cause is the effect of overtraining, since according to Fonberg et al. (1962) it prevents the effects of the lesion on the amygdala. At the same line, Thatcher & Kimble, (1966) showed no effect on the retention of a learned avoidance response after overtraining. In contrast, a recovery deficit is observed in absence of overtraining (Goldstein, 1974; Thatcher & Kimble, 1966). It is possible to observe a very similar case in inhibitory avoidance. Reversibly inactivation or lesion to the amygdala affects retention if it is done soon after the training, but has no effect if it is performed much later (Liang et al., 1982; McGaugh et al., 2000; Parent & McGaugh, 1994; Wilensky et al., 2000; 2006).

However, although the amygdala is believed to be essential for the acquisition of Pavlovian fear conditioning, studies using excitotoxic lesions have recently called this view into question. Thus, different nuclei of the amygdala could contribute to the modulation of memory consolidation of an avoidance response (active or passive) in a different way:

  1. Pallial amygdala. Lesions to the basolateral nucleus (lateral, basal, and accessory basal) produce severe deficits in the acquisition of both active and passive avoidance, although the effects on retention are lower in the passive than in the active (Ambrogli et al., 1991). The same lesions have no effect on the conditioned response nor in a passive avoidance response with contextual cues (Selden et al., 1991). A previous study comparing the effects of electrolytic lesions to those produced by ibotenic acid showed that only the electrolytic lesions by radiofrequency impairs for an active avoidance response (Jellestad & Cabrera, 1986). Nevertheless, this study did not define what amygdalar structures were indeed damaged. Moreover, it postulates the idea of the involvement of a pathway through the nucleus instead of the cell groups present in those structures.

  2. Subpallial amygdala. Lesions to the central nucleus produce deficits in both an active avoidance response (Riolobos & Garcia, 1987) and a two-way active avoidance (Sánchez-Riolobos, 1986).

All these data together support the differential involvement of pallial and subpallial nuclei in active avoidance learning (McGaugh et al., 2000; Wilensky et al., 2000; 2006).

3.6. Effects of electrical stimulation

Early studies showed that electrical stimulation of the amygdala induced amnesia for different learning processes (Grossman, 1972; Isaacson 1976; Kaada, 1972) included avoidance learning. The specific stimulation of the central nucleus, immediately after training in an avoidance task, produced a large deficit in the retention of that task and a blockade of fear conditioning (Gold et al., 1975; McDonough & Kesner, 1971). The same results were observed in the retention of passive avoidance tasks (Gold et al, 1973a; Kesner, 1982), and in a one-way active avoidance after unilateral stimulation in the basomedial nucleus (McGaugh & Gold 1974). Gold et al. (1973) showed that 1 hour after training, stimulation produced a deficit in the avoidance response, but 6 hours later produced no effect in the same avoidance test. This data suggests that there is a plastic phenomenon related to learning, which would be disrupted by the stimulation shortly after training, but not once its effects are consolidated. Other studies also described amnesic effects in both one-way avoidance and discriminated avoidance (press a lever) after post-training stimulation (Hanwerker et al., 1974; McGaugh & Gold, 1976). Nevertheless, other studies have found memory facilitating effects after stimulation in passive avoidance tests with a weak shock (Gold & Van Buskirk, 1975). In other studies, a low intensity shock showed similar results in tasks such as conditioned emotional response. Lidsky et al. (1970), Gold & McGaugh (1975), and McGaugh & Gold (1976) proposed that the different motivational state caused by a severe or a mild shock condition would produce the differential effect of electrical stimulation. Subsequent studies have exposed as the amnesic effects of electrical stimulation can be modulated by hormone levels, which would support this hypothesis. The removal of the adrenal gland (decline on systemic levels of catecholamines) showed that electrical stimulation does not induce amnesia but showed an improvement in the retention of an inhibitory avoidance response in both active and passive condition (Bennett et al., 1985). Also, in a similar study, Liang et al. (1985) injected norepinephrine immediately after training and just before intraamygdaline electrical stimulation. Animals without adrenal medulla showed the same deficits as the control animals, which could determine a modulation of systemic norepinephrine on memory through or in connection with the amygdala.

In fact, we know the involvement between the amygdala (mainly central nucleus) and the CHR (corticotrophin releasing hormone) - ACTH (adrenocorticotropic hormone) -corticosteroids cascade and norepinephrine release, and its correlation with the response of fear, anxiety and stress (Davis 1992). Several studies have linked the conditioning of stressful situations, amygdalar lesions and intraamygdaline inoculation of systemic ACTH or CHR. Bush et al. (1973) showed that an electrolytic lesion of the amygdala produced extensive damage to a passive avoidance response, and this effect was reversed by systemic injection of ACTH. Krivanek (1971) showed that injection of norepinephrine, pentylenetetrazole (GABAergic antagonist) and ACTH produced a facilitation of avoidance behavior. Moreover, in an experiment with adrenalectomized rats, intra amygdalin electrical stimulation produced an amnesic effect in active and passive avoidance in control animals, while animals without adrenals improved their performance and retention in these tasks (Bennett et al., 1985). Another series of studies have combined individual differences in avoidance tasks and hormone action in the amygdala. Wiersma et al. (1998) determined that the animals of the RHA strain (high rate of avoidance) and the RLA (low avoidance rate) had different behavioural, physiological, and neurobiological responses under stress-free conditions after CRH microinfusion into the central nucleus of the amygdala. RHA increased heart-rate activity and decreased resting only in a stressful situation (inescapable shock) while a slight behavioral activation was observed in RLA. These results show a correlation between the ability to learn avoidance tasks, intra-individual differences, and hormonal regulation in the amygdala in an emotional context.

3.7. Social and neuroimage studies of primates and humans

In the studies of mammals (see above) it appears that the amygdala is involved in normal (LeDoux, 2012; Parkes & Westbrook, 2011; Phelps & LeDoux, 2005) and pathological (Magdaleno-Madrigal et al., 2010, Roozendaal et al., 2009) emotional processing. In primates including humans it integrates more complex functions of social and cognitive nature: such as anxiety disorders (Holzchneider & Mulert, 2011; Kim et al., 2011), decision making (Seymour & Dolan, 2008) or fear, and social learning (Olsson & Phelps, 2007). In species with a highly complex social environment, like in the human case, the amygdala has a crucial role. Neuroimaging studies has been shown that the amygdala functions as a relevance detector that allows humans to perceive incongruence in the emotional expressions, or fear (Phelps & LeDoux, 2005), although others argue that the amygdala activation is more indirect in these cases (van der Gaag et al., 2007). In humans, the amygdala shares common functions with other species, and also acquires more subtle properties in the management of emotional content information that can be shared at least in part with other social primates (Pessoa & Adolphs, 2010), in which circuit model "low road" and "high road" of emotional processing becomes more complicated in terms of increased complexity of sensory processing and perception in humans and primates, taking in this case a greater involvement of the cortex. However, there is a general conservation of function, with an implementation of new features that accompany human neural development itself (Adolphs, 2009; LeDoux, 2012; Olsson & Phelps, 2007; Pessoa & Adolphs, 2010). Likewise, in the pathological aspect of emotion, fMR studies have shown correlated changes in volume of the amygdala and secretion of cortisol in psychiatric disorders such as unipolar depression (Schuhmacher et al. 2012) and other behavioral disorders as described in other chapters of the present book.


4. Function of the amygdala homologous in non mammals vertebrates

Lesions or stimulation of the amygdala in reptiles and birds (or structures considered homologous to the amygdala) produce changes in social behavior or learning processes (Martínez-García et al, 2007). These changes are similar and show a comparable function to the amygdalar system of mammals. In the case of crocodilian reptiles (Caiman sclerops), lesions of the amygdala results in decreased frequencies of aggressive patterns (Keating et al., 1970). Likewise, lesions to the areas considered homologous to the amygdala in a iguanide in a social environment (Sceloporus occidentalis) caused a syndrome similar to that of mammals as it produced deficits in attention and response (loss of initiative), in patterns of dominance and submission, and a decrease in the response to fear stimulus (Tarr, 1977). Reproductive and aggressive behaviors, as well as associated seasonal variations, have been the main object of study in snakes (Thamnophis sirtalis parietalis). These studies show that the sphericus, considered homologous to the amygdala in these reptiles (Bruce & Neary, 1995; Sriedter, 1997), presents sexual dimorphism which is more evident of the males (Crews et al., 1993). Moreover, when the nucleus sphericus is lesioned before the start of the stage of hibernation, there is a facilitation of courtship patterns in the male after the hibernation that correlates with increased blood levels of androgens, indicating a potential facilitating effect of the lesion (Krohner & Crews, 1987).

Zeier & Karten (1971) have argued that the posteromedial portion of the archistriatum, now called arcopallium (The Avian Brain Nomenclature Consortium, 2005), is the homologous to pallial amygdala (basolateral amygdala) in birds. The experimental results support the homology proposal (Dafters, 1975; Goodson & Bass, 2001; Lowndes & Davies, 1994).

In the case of the turtle dove (Streptopelia risoria), it is known that electrical stimulation of archipallium produces emotional responses of fear, offense, and defense (The Avian Brain Nomenclature Consortium, 2005; Vowles & Beasley, 1974). In addition, lesions to this structure abolish the conditioned emotional response (as the cardiac acceleration that occurs paired with a shock) in Columba livia (Cohen, 1975, Dafter, 1976). When an active avoidance is used, the arquipallial lesion produces the same deficit for the acquisition of a avoidance response that the lesion of the mammalian amygdala (Dafter, 1975). In the case of active avoidance, the arquipallial lesion produces the same deficit in the acquisition of the avoidance response that lesion of the mammalian amygdala (Dafter, 1975). Phillips & Youngren (1968) showed that unilateral excitotoxic lesions of this structure in chicks that are 5 days old showed a decrease in distress vocalizations (the chirp). Anatides have a similar effect, since in the mallard (Anas platyrhynchos) lesions to archipallium produce a generalized effect as defined by author of "domestication" or put in another way, lack of fear of emotional reactivity (Phillips, 1964; The Avian Brain Nomenclature Consortium, 2005). The same effect occurs in Columba livia after lesions of the posterior portion of archipallium. In contrast, lesions to the anterior portion facilitate the emotional reaction of fear (Zeier, 1971). In a study in chickens (Gallus gallus), Maser et al. (1973) showed that lesions to the anterolateral portion produced an increase in reactive immobility typical of fear responses. In psittacidae (Agapornis roseicolis), lesions of the medial part induces a decrease of fear, and it facilitates the approach toward dangerous stimuli of the animal (Phillips, 1968). These results seem to clearly differentiate two portions of the birds’ medial archipallium, with opposite functions from the point of view of control of emotional responses. This is corroborated by the results of a study of a fringillidae, the zebra finch (Taenopigya guttata). In this study the activity of brain areas was measured by the uptake of 2-deoxyglucose-C14, after subjecting male animals to various stressful circumstances (Bischof & Herrmann, 1986). One group was housed alone in a cage. Animals with experience in courtship were assigned to a second group. A third group of subjects did not have experience in courtship and a fourth group was subjected to a situation in which the experimenter pretended to try to catch them in their cages. The analysis showed a high rate of uptake in the caudal portion of archistriapallium in the group without experience in courtship and the one of capture inside the cage: the two most stressful situations. Also lesions to the taenia nucleus of the amygdala (homologous to part of the medial amygdala of mammals) seriously affect the socio-sexual behavior of male Zebra finches (Ikebuchi et al., 2009).

In the case of teleosts fish, the results from the experiments of telencephalic lesions and stimulation that produce alterations in reproductive and aggressive behaviors (de Bruin, 1980; Kyle & Peter, 1982; Kyle et al., 1982) present a picture of behavioral changes that can be easily compared to changes mediated by the amygdala function. For instance, the agonistic behavior of male Betta fish has been widely studied. The sight of another male typically stimulates a series of agonistic behavioral displays toward the intruder often followed by physical aggression. The context used in these studies is known as agonistic context. The partial ablation of the dorsomedial telencephalon (Dm) in Betta splendens produces a loss of reactivity (facilitation of habituation) in an agonistic context (Marino-Neto & Sabbatini, 1983). However, lesion experiments often extend the damage to the basal portion of Dmv. If we admit the existence of telencephalic structures with limbic function equivalent to those of tetrapods, we would also have to admit that lesions in different limbic areas produce similar effects in fish and tetrapods.

The results of ablation studies in teleost fish show that the Dmv region, proposed as homologous to the pallial amygdala of land vertebrates, has a key role in Pavlovian conditioning. These studies showed a clear lesion effect in both the acquisition and maintenance of a two-way active avoidance behavior (Portavella et al., 2004a, 2004b; Portavella & Vargas, 2005). Thus, lesions to the Dmv region produce a deficit equivalent to those described in the case of complete ablation of the telencephalon in earlier studies in Pavlovian conditioning (Aronson, 1948; de Bruin, 1977; 1980; Fiedler, 1967; 1968; Hale, 1956; Kamrin & Aronson, 1954; Karamyan et al., 1967; Kassel & Davis, 1977; Kassel et al., 1976; Noble, 1939; Noble & Bourne, 1941; Overmier & Gross, 1974;; Segaar, 1961; 1965; Segaar & Nieuwenhuys, 1963; Ribbink, 1972). Also, the deficit showed in both the acquisition and retention in avoidance behavior cannot be attributed to the lack of activity or initiative of the animal after lesion, because the level of escape is very high. In addition, the absence of effects on spatial memory or motor response (Portavella & Vargas, 2005) rules out a possible functional homology with the hippocampus and basal ganglia of tetrapods (Braford, 1995; Braford et al.,1992; 1993; Echteler & Saidel, 1981; Murakami et al., 1983; Nieuwenhuys & Verrijdt, 1983; Northcutt, 1995; Northcutt & Braford, 1980; Parent, 1986; Parent et al., 1978). Thus, we concluded that the lesion produced a deficit in the associative process between the discriminative stimulus and the shock (Portavella et al, 2002; 2004a, 2004b; Portavella & Vargas, 2005; Vargas et al., 2009). Other results in fear context conditioning have showed that lesions of the dorsomedial telencephalic portion in Betta splendens produced a facilitation of habituation to the context (Marino-Neto & Sabbatini, 1983) and variations in levels of aggression (de Bruin, 1980). Taken as a whole, these data indicate that the Dm telencephalon area shares a great similarity with pallial amygdaloid nuclei and homologous structures in reptiles (Crews et al., 1993; Keating et al., 1970; Krohner & Crews, 1987; Tarr, 1977), birds (Cohen, 1975; Dafter, 1975; 1976; Ikebuchi et al., 2009; Martínez-García, et al., 2002; Phillips 1968; Phillips & Youngren, 1968; Vowles & Beasley, 1974; Zeier, 1971), and mammals (Ambrogli et al, 1991; Fonberg, 1973; Grossman et al., 1974; Hanwerker et al., 1974; Horvath, 1963; Killcross et al., 1997; Liang & McGaugh, 1983; McIntery & Stein, 1973; Pellegrino, 1968; Roozendaal et al., 1993; Sanchez-Riolobos, 1986; Takashina et al., 1995; van-der-Zee et al., 1997; Werka et al., 1978; Wiersma et al., 1998). These amygdala lesions affect not only the avoidance conditioning, but also the fear conditioning in mammals and birds (Cohen, 1975; Dafter, 1976).

One of two main approaches on the theories of avoidance in fish (Flood et al., 1976; Zhuikov et al., 1994) is a model adapted from the theory of the two processes of Mowrer (1947). This model recognizes the existence of a two processes. One of them is the conditioning process of a motivational state (fear). That is crucial to the Pavlovian conditioning. The other one is the association between the CS and the shuttling response (Zhuikov et al, 1994). Given these results, it could be postulated that the lesion in the dorsomedial region deprives the fish of such capacity, and it would be one of the causes of the main deficit for the maintenance of avoidance behavior (Portavella et al, 2002; 2004a, 2004b; Portavella & Vargas, 2005; Vargas et al., 2009).


5. Conclusion

Learning theories for the function of the amygdalar system are not an organized body of various alternatives, but show a set of nuclei that receive any type of sensory or perceptual relevant information inducing changes in the neuroendocrine system, and the emergence of emotional patterns mediated by this structure (autonomic, humoral, and behavioral). This set of nuclei would in turn form a central part of the emotional learning processes (Aggleton, 1992; Davis, 1992; Gallagher & Chiba, 1996; Gallagher & Holland, 1992; Halgren, 1992; Killcross et al., 1997; LeDoux, 1992; 1995; Olsson & Phelps, 2007; Phelps & Anderson, 1997). Likewise, though being intrinsically a very complex structure (Amaral et al., 1992; Pitkänen et al., 1997), it is clear that lesions of a large part of the nucleus of the pallial amygdala (basolateral amygdala) and also the subpallial part seriously affect all type of emotional learning. In fish, the ablation of Dmv telencephalon induced a clear deficit in a conditioned avoidance behavior, similar to that produced after a complete ablation of the telencephalon (Portavella et al., 2004a, 2004b; Portavella & Vargas, 2005; Vargas et al.,2009). These data coupled with the effects of Dm lesions on aggressive behavior, breeding, habituation in situations of aggression in a resident/intruder paradigm (de Bruin, 1980; Marino-Neto & Sabbatini, 1983), as well as data from electrical stimulation of Dm in Carassius that show facilitation and inhibition of aggressive and reproductive patterns or startle response and escape (Savage, 1971), support the homology of the fish telencephalic Dmv with the pallial amygdala of mammals. This idea have been proposed on the basis of neuroanatomical and neurohistochemical evidence of similarities between the two structures developing an evolution-based model of brain organization (Braford, 1995; Echteler & Saidel, 1981; Hornby et al., 1987; Ito et al., 1986; Medina & Reiner, 1995; Murakami et al., 1983; Northcutt, 1995; 2008; Piñuela & Nortcutt, 1994; Reiner & Northcutt, 1992; Striedter, 1991; Wulliman & Rink, 2002) and that of reptiles (Crews et al., 1993; Keating et al., 1970; Krohner & Crews, 1987; Tarr, 1977), birds (Cohen, 1975; Dafter, 1975; 1976; Ikebuchi et al., 2009; Phillips 1968; Phillips & Youngren, 1968; Vowles & Beasley, 1974; Zeier, 1971), and mammals (Ambrogli et al., 1991; Fonberg, 1973; Grossman et al., 1974; Hanwerker et al., 1974; Horvath, 1963; Killcross et al., 1997; Liang & McGaugh, 1983; McIntery & Stein, 1973; Pellegrino, 1968; Roozendaal et al., 1993; Sanchez-Riolobos, 1986; Takashina et al., 1995; van-der-Zee et al., 1997; Werka et al., 1978; Wiersma et al., 1998).

This exhibition along with the data of the previous sections would support the fact that structures homologous to the amygdala of the different groups of vertebrates, including humans, share similar functions, at least in terms of information processing of emotional content, which is essential for the survival of the species (LeDoux, 2012). This idea is based on results from genoarchitectonical studies showing the consistancy of genetical markers along vertebrates’ brains evolution. In the case of amygdala of tetrapods (Medina et al., 2011) is composed of four different regions: ventral pallial amygdala (i.e. basal amygdala of mammals, dorsal ventricular ridge in reptiles and birds), striatal amygdala (i.e. the central nucleus in different groups), pallidal amygdala (medial amygdala of amniotes) and hypothalamical part present in different vertebrates groups (i.e. bed nucleus and extended amygdala). A part of specific gene expression of these four divisions is present in mammals, birds, reptiles, and amphibians. In the case of teleost fish, behavioral approaching (Portavella et al., 2004a, 2004b; Portavella & Vargas, 2005) showed similar learning deficits after brain lesions on homologues areas to mammalian amygdala, and genetical studies showed constancy in the expression of pallial and subpallial genes, and the presence of, at least, a medial amygdala (Gonzalez & Northcutt, 2009) and the hypothalamical components (Eaton et al., 2008). The behavioral studies commented in previous sections of this chapter show how essential functions for species survival such as fear conditioning, escape and avoidance behavior, aggressive, and sexual behaviors are dramatically impaired after mammalian amygdala lesions, or homologues structures in the case of birds, reptiles, amphibians, or teleost fish (see sections II and III of this chapter). These behavioral data and genetical studies, together with evidence of homologies seem to support the existence of a basic bauplan in the vertebrates’ line, including man, which has been broadly conserved during evolution of the vertebrate nervous system, including structures such as the amygdala.


This study was supported by PSI2009-12761 and RyC2006/1284 (Spanish Government) grants. We thank Paola Revilla for technical assistance and Brittany Adams for her helpful comments on the manuscript.


  1. 1. AdolphsR2009The social brain: neural basis of social knowledgeAnnual Reviews of Psuychology, 60693716
  2. 2. AdolphsRGosseinFBuchananT. WTranelDSchynsPDamasioA. R2005A mechanism for impaired fear recognition after amygdala damageNature, 4336872
  3. 3. AdolphsRTranelDDamasioHDamasioA1994Impaired recognition of emotion in facial expressions following bilateral damage to human amygdala.Nature372669672
  4. 4. AggletonJ. P1985A description of intraamygdaloid connections in the old world monkeys, Experimental Brain Research, 57390399
  5. 5. AggletonJ. P1992The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction.Wiley-Liss, New York.
  6. 6. AmanoTDuvarciSParéD2010The basal nuclei of the amygdala are involved in conditioned fear extinction but not expression. Society for Neuroscience Abstract, 36, 808, 24
  7. 7. AmaralD. GPriceJ. LPitkänenACarmichaelS. T1992Anatomical organization of tje primate amygdaloid complex. In: J. P. Aggleton (Ed.). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York.
  8. 8. Ambrogi-lorenziniCBucherelliCGiachettiAMugnaiLTassoniG1991Effects of nucleus basolateralis amygdalae neurotoxic lesions on aversive conditioning in the rat.Physiology and Behavior, 49765770
  9. 9. AronsonL. R1948Problems in the behavior and physiology of a species of African mouthbreeding fish. Transactions of the New York Academy of Sciences, 113342
  10. 10. BennettCLiangK. CMcgaughJ. L1985Depletion of adrenal catecholamines alters the amnestic effect of amygdala stimulation.Behavioral Brain Research, 158391
  11. 11. BischofH. JHerrmannK1986Arousal enhances 14C2-deoxyglucose uptake in four forebrain areas of the zebra finch. Behavioral Brain Research, 21215221
  12. 12. BlanchardD. CBlanchardR. J1972Innate and conditioned reactions to threat in rats with amygdaloid lesions.Journal of Comparative and Physiological Psychology81281290
  13. 13. BlissT. V. PCollingridgeG. L1993A synaptic model of memory: long-term potentiation in the hippocampus.Nature3613139
  14. 14. BradyJ. VSchreinerLGellerJKlingA1954Subcortical mechanisms in emotional behavior: The effect of rhinencephalic injury upon acquisition of a conditioned avoidance response in cats.Journal of Comparative and Physiological Psychology47179196
  15. 15. BrafordM. R1995Comparative aspects of forebrain organization in ray-finned fishes: touchstones or not? Brain Behavior and Evolution, 46259274
  16. 16. BrafordM. RJensenA. ARussellR. W1992Some connections of the torus longitudinalis in the osteoglossomorph teleost, Xenomystus nigri. Society for Neuroscience Abstracs, 18, 326.
  17. 17. BrafordM. RPrinceEMccormickC. A1993A presumed acoustic pathway from the ear to the telencephalon in an osteoglossomorph teleost. Society for Neuroscience Abstracs, 19, 160.
  18. 18. BruceL. LNearyT. J1995The limbic system of tetrapods: A comparative analysis of cortical and amygdalar populationsBrainBehavior and Evolution, 46224234
  19. 19. BukasiGBickfordR. GPonomareffGThalL. JMandelRGageF. H1988Nucleus basalis and thalamic control of neocortical activity in freely moving rat. Journal of Neuroscience, 840074026
  20. 20. BushD. FLovelyR. HPaganoR. R1973Injection of ACTH induces recovery from shuttle-box avoidance deficits in rats with amygdala lesions. Journal of Comparative and Physiological Psychology, 83168172
  21. 21. CalvoJ. MBadilloSMorales-ramírezMPalacios-salasP1987The role of the temporal lobe amygdala in ponto-geniculo-occipital activity and sleep organization in cats.Brain Research4032230
  22. 22. CampeauSDavisM1995Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiates startle in rats trained concurrently with auditory and visual conditioned stimuli.Journal of Neurociences, 1523012311
  23. 23. CampenotR. B1969Effect of amygdaloid lesions upon active avoidance acquisition and anticipatory responding in rats.Journal of Comparative and Physiological Psychology69492497
  24. 24. CaruthersR. P1969Deficits in shock-avoidance performance after amygdala-hippocampus separation.Journal of Comparative and Physiological Psychology67547554
  25. 25. ChanconieMClairrambaultP1975Développment du télencephale de Salmo irideus Gib. Journal of Comparative Neurology, 208107126
  26. 26. ChapmanP. FBellavanceL. L1992NMDA receptors-independent LTP in the amygdala. Synapse, 8145149
  27. 27. ClugnetM. CLeDoux, J. E. & Morrison S. F. (1990Unit responses evoked in the amygdala and striatum by electrical stimulation of the medial geniculate body.Journal of Neuroscience, 1010551061
  28. 28. CohenD. H1975Involvement of the avian amygdala homologue (archistriatum posterior and mediale) in defensively conditioned heat rate change. Journal of Comparative Neurology, 1601336
  29. 29. CousensGOttoT1998Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning.Behavioral Neuroscience11210921103
  30. 30. CrewsDRobkerRMendocaM1993Seasonal fluctuations in brain nuclei in the red-side garter snake and their hormonal control.Journal of Neuroscience, 1353565364
  31. 31. DaftersR1975Active avoidance behavior following archistriatal lesions in pigeons.Journal of Comparative and Physiological Psychology8911691179
  32. 32. DaftersR1976Effect of medial archistriatal lesions on the conditioned emotional response and on auditory discrimination performance of the pigeon.Physiology and Behavior, 17659665
  33. 33. DavisM1992The role of the amygdala in conditioned fear. In: J. P. Aggleton (Ed.). The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York. 55305
  34. 34. DavisM2000The role of the amygdala in conditioned and unconditioned fear and anxiety. In: J. P. Aggleton (Ed.). The Amygdala. Oxford University Press, Oxford, UK. 213288
  35. 35. De BruinJ. P. C1977Telencephalic functions in the behavior of the Siamese fighting fish,Betta splendens Regan (Pisces, Anabantidae). PhD Dissertation. University of Amsterdam.
  36. 36. De BruinJ. P. C1980Telencephalon and behavior in teleost fish. A neuroethological approach. In S. O. E. Ebbesson (Ed.). Comparative neurology of the telencephalon. Plenum, New York. 175201
  37. 37. DeolmosJAlheidG. FBeltraminoC. A1985Amygdala. In: G. Paxinos (Ed.). The rat nervous system. 1Academic Press, New York. 223334
  38. 38. DiCaraL., Braun, J. J. & Pappas, B. (1970Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal the neocortex in the ratJournal of Comparative and Physiological Psychology73208216
  39. 39. DudekS. MBearM. F1992Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade.Proceedings of National Academy of Sciences, 8943634367
  40. 40. DuvarciSPopaDParéD2011Central amygdala activity during fear conditioningJournal of Neurosciences, 31289294
  41. 41. EatonJ. LHolmqvistBGlasgowE2008Ontogeny of vasotocin-expressing cells in zebrafish: selective requirement for the transcriptional regulators orthopedia and singleminded 1 in the preoptic area. Developmental Dynamics, 2379951005
  42. 42. EchtelerS. MSaidelW. M1981Forebrain projections in the goldfish support telencephalic homologies with land vertebrates. Science, 212683685
  43. 43. FallsW. AMiserendinoM. J. DDavisM1992Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala.Journal of Neuroscience, 12854863
  44. 44. FanselowM. SKimJ. J1994Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphono-valeric acid to the basolateral amygdalaBehavioral Neuroscience108210212
  45. 45. FarbC. RLeDoux, J. E. (1997NMDA and AMPA receptors in the lateral nucleus of the amygdala are postsynaptic to auditory thalamic afferents.Synapse, 27106121
  46. 46. FerryBMcgaughJ. L2008Involvement of basolateral amygdala alpha2-adrenoceptors in modulating consolidation of inhibitory avoidance memory.Learning and Memory, 323843
  47. 47. FiedlerK. L1967Ethologische und neuroanatomische Auswirkungen von Vorderhirnexstirpationen bei Meer brassen (Diplodus) and Lippfischen (Crenilabrus, Perciformes, Teleostei). Journal für Hirnforschung, 9481563
  48. 48. FiedlerK. L1968Verhaltenswirksame Strukturen im Fischgehirn. Zoologischer Anzeiger, 31602616
  49. 49. FloodN. BOvermierJ. BSavageG. E1976The teleost telencephalon and learning: An interpretative review of data and hypotheses. Physiology & Behavior, 16783798
  50. 50. FlorescoS. BToddC. LGraceA. A2001Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons.Journal of Neuroscience, 21491522
  51. 51. FonbergE1973The normalizing effect of lateral amygdalar lesions upon dorsomedial amygdalr syndrome in dogs. Acta Biologiae Experimentalis, 33449466
  52. 52. FonbergEBrutkowskiSMempel (1962Defensive conditioned reflexes and neurotic motor reactions following amygdalectomy in dogs.Acta Biologiae Experimentalis225157
  53. 53. Fusar-poliPPlacentinoACarlettiFAllenPLandiPAbbamonteMBaraleFPerezJMcguirePPolitiP. L2009Laterality effect on emotional facesprocessing: ALE meta-analysis of evidence. Neuroscience Letters, 452262267
  54. 54. GageS. P1893The brain of Diemyctylus viridescens from larval to adult life and comparison with the brain of Amia and Petromyzon. In: Wilder Quarter Century Book. Ithaca, New York.
  55. 55. GallagherMChibaA1996The amygdala and emotion. Current Opinion in Neurobiology, 6221227
  56. 56. GallagherMHollandP. C1992Understanding the function of the central nucleus: Is simple conditioning enough?. In: J. P. Aggleton. (Ed.). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, 307321
  57. 57. GeanP. WChangF. CHuangC. CLinJ. HWayL. J1993Long-term enhancement of EPSP and NMDA receptor-mediated synaptic transmission in the amygdala.Brain Research Bulletin31711
  58. 58. GewirtzJ. CDavisM1997Second-order fear conditioning prevented by blocking NMDA receptors in amygdala.Nature388471473
  59. 59. GhiasvandMRezayofAZarrindastM. RAhmadiS2011Activation of cannabinoid CB1 receptors in the central amygdala impairs inhibitory avoidance memory consolidation via NMDA receptorsNeurobiology of Learning and Memory96333338
  60. 60. GoldP. EHanskinsLEdwardsRChesterJMcgaughJ. L1975Memory interference and facilitation with posttrial amygdala stimulation: Effect on memory varies with footshock level.Brain Research86509513
  61. 61. GoldP. EMacriJMcgaughJ. L1973aRetrograde amnesia gradients: Effects of direct cortical stimulation.Science, 17913431345
  62. 62. GoldP. EMacriJMcgaughJ. L1973bRetrograde amnesia produced by subseizure amygdala stimulation.Behavioral Biology9671680
  63. 63. GoldP. EMcgaughJ. L1975ASingle-tracetwo-process view of memory storage processes. In: D. Deutsch & A. J. Deutsch (Eds.). Short Term Memory. Academic Press, New York.
  64. 64. GoldP. EVan BuskirkR. B1975Facilitation of time-dependent memory processes with posttrial epinephrine injections.Behavioral Biology13145153
  65. 65. GoldsteinM. L1974The effect of amygdalectomy on long-term retention of an undertrained classically conditioned fear response. Bulletin of Psychonomic Society, 4548550
  66. 66. GonzálezANorthcuttR. G2009An immunohistochemical approach to lungfish telencephalic organizationBrainBehavior and Evolution, 744355
  67. 67. GoodsonJ. LBassA. H2001Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates.Brain ResearchReviews, 35246265
  68. 68. GrossmanS. P1972The role of the amygdala in escape-avoidance situations. In: B. E. Eleftheriou (Ed.). The Neurobiology of the Amygdala. Advances in Behavioral Biology, 2Plenum Press, New York, 537551
  69. 69. GrossmanS. PGrossmanLWalshL1974Functional organization of the rat amygdala with respect to avoidance behavior.Journal of Comparative and Physiological Psychology88829850
  70. 70. HaleE. B1956Effects of forebrain lesions on the aggressive behavior of green sunfish. Lepomis cyanellusPsysiological Zoology, 29107127
  71. 71. HalgrenE1992Emotional neurophysiology of the amigdala within the contex of human cognition. In: J. P. Aggleton (Ed.). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, 191228
  72. 72. HandwerkerMGoldP. EMacGaugh, J. L. (1974Effects of posttrial electrical stimulation of the amygdala on retention of an active avoidance response. Brain Research, 75324327
  73. 73. Hebb D. O. (1949). The Organization of Behavior, Wiley: New York.
  74. 74. HelmstetterF. JBellgowanP. S1994Effects of the muscimol applied to de basolateral amygdala in acquisition and expression of contextual fear conditioning in rats. Behavioral Neuroscience10810051009
  75. 75. HelmstetterF. JParsonsR. GGaffordG. M2008Neurobiology of Learning of Memory, 89324337
  76. 76. HerryCCiocchiSSennVDemmouLMüllerCLüthiA2008Switching on and off fear by distinct neuronal circuits. Nature, 454600606
  77. 77. HerzogCOttoT1998Contributions of anterior perirhinal cortex to olfactory and contextual fear conditioning.Neuroreport9185559
  78. 78. HicksT. P1995The role of glutamate receptor and its receptors in synaptic transmission. In: T. W. Stone (Ed.). CNS Neurotransmitters and Neuromodulators: Glutamate. CRS Press, Boca Raton, Florida, 201218
  79. 79. HolzschneiderKMulertC2011Neuroimaging in anxiety disordersDialogues in Clinical Neuroscience13453461
  80. 80. HornbyPPiekutD. TDemskiL. S1987Localization of immunoreactive tyrosine hydroxylase in the goldfish brain.Journal of Comparative Neurology, 261114
  81. 81. HorvathF. E1963Effects of basolateral amygdalectomy on three types of avoidance behavior in cats. Journal of Comparative and Physiologycal Psychology, 56380389
  82. 82. Hunsaker MR & Kesner RP2008Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fearNeurobiology of Learning & Memory, 896169
  83. 83. IkebuchiMHasegawaTBischofH. J2009Amygdala and socio-sexual behavior in male zebra finchesBrainbehavior and Evolution, 74250257
  84. 84. IsaacsonR. I1976Experimental brain lesions and memory. In: M. R. Rosenzweigand E. L. Bennet (Eds.). Neural mechanisms of learning and memory. The MIT Press, Cambridge, Massachusetts.
  85. 85. ItoHMurakamiTFukuokaTKishidaR1986Thalamic fiber connections in a teleost (Sebastiscus marmoratus): Visual somatosensory, octavolateral, and cerebellar relay region to the telencephalon.Journal of Comparative Neurology, 250215227
  86. 86. JarrelT. WGentileC. GRomanskiL. MMccabeP. MSchneidermanN1987Involvement of cortical and thalamic auditory regions in retention of differential bradycardia conditioning to acoustic conditioned stimuli in rabits. Brain Research, 412285294
  87. 87. JellestadF. KCabreraI. C1986Exploration and avoidance learning after ibotenic acid and radio-frequency lesions in the rat amygdala.Behavioral and Neural Biology46195215
  88. 88. JiJMarenS2008Lesions of the entorhinal cortex or fornix disrupt the context-dependence of fear extinction in ratsBehavioral Brain Research, 1942016
  89. 89. JohansenJ. PCainC. KOstroffL. ELeDoux,J. E. (2011Molecular mechanism of fear learning and memory.Cell28509524
  90. 90. KaadaB. R1972Stimulation and regional ablation of the amygdaloid complex with reference to functional representations. In: B. E. Eleftheriou (Ed.). The Neurobiology of the Amygdala. Advances in Behavioral Biology, 2Plenum Press, New York, 205281
  91. 91. KamrinR. PAronsonL. R1954The effects of forebrain lesions on mating behavior in the male platyfish, Xiphophorus maculatus. Zoologica, 39133140
  92. 92. KappB. SPascoeJ. PBixlerM. A1984The amygdala: a neuroanatomical system approach to its contributions to aversive conditioning. In: N. Butlersand & L. R. Squire (Eds.). Neuropsychology of Memory. Guilford Press, New York, 473488
  93. 93. KappB. SWhalenP. JSuppleW. FPascoeJ. P1992Amygdaloid contributions to conditioned arousal and sensory information processing. In: J. P. Aggleton (Ed.). The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, 229254
  94. 94. KappB. SWilsonAPascoeJ. PSuppleW. FWhalenP. J1990A neuroanatomical systems analysis of conditioned bradycardia in the rabits. In: M. Gabrieland & J. Moore (Eds.). Learning and computational neuroscience: foundations of adaptative networks. MIT Press, Cambridge, Massachussett, 5390
  95. 95. KaramyanA. IMalukovaI. VSergeevB. F1967Participation of the telencephalon of bony fish in the accomplishment of complex conditioned-reflex and general behavior reactions. In Behavior and Reception in Fish. Academy of Science, USSR, Moscow (translated by Bureau of Sport Fisheries and Wildlife, EEUU).
  96. 96. Kassel, J. & Davis, R. E. (1977). Recovery of function following simultaneous and serial telencephalon ablation. Behavioral Biology, 21 489499 .
  97. 97. KasselJDavisR. ESchwagmeyerP1976Telencephalic lesions and behavior in the teleost Macropodus opercularis: further analysis of reproductive and operant behavior in the male.Behavioral Biology, 18179188
  98. 98. KeatingG. EKormannSHorelA1970The behavioral effects of stimulating and ablating the reptilian amygdala. Physiology and Behavior, 55559
  99. 99. KeeneC. SBucciD. J2008Neurotoxic lesions of retrosplenial cortex disrupt signaled and unsignaled contextual fear conditioningBehavioral Neurosciences, 12210707
  100. 100. KembleE. DBlanchardD. CBlanchardR. J1990Effects of regional amygdaloid lesions of flight and defensive behaviors of wild black rats (Rattus rattus).Physiology and Behavior, 4815
  101. 101. KembleE. DBlanchardD. CBlanchardR. JTakushR1984Taming in wild rats following medial amygdaloid lesions.Physiology and Behavior, 32131134
  102. 102. KesnerR. P1982Brain stimulation: Effects on memory.Behavioral Brain Biology, 36315367
  103. 103. KillcrossSRobbinsT. WEverittB. J1997Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala.Nature388377380
  104. 104. KimM. JLoucksR. APalmerA. LBrownA. CSolomonK. MMarchanteA. NWhalenP. J2011The structural and finctional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research, 223403410
  105. 105. KimY. SStumpfW. ESarM1978Topography of estrogen target cells in the forebrain of goldfish, Carassius auratus.Journal of Comparative Neurology, 197611620
  106. 106. Kling, A. J., Orbach, J., Schwartz, N. & Towne, J. (1960). Injury to the limbic system and associated structures in cats. Archives of General Psychiatry, 3 391340 .
  107. 107. KlingA. SBrothersL. A1992The Amygdala and Social Behavior. In: J. P. Aggleton (Ed.). The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, 353377
  108. 108. KlüverHBucyP. C1939Preliminary analysis of the temporal lobes in monkeys. Archives of Neurology and Psychiatry, 429791000
  109. 109. KrivanekJ1971Facilitation of avoidance learning by pentylenetetrazol as a function of task difficulty, deprivation and shock level.Psychopharmacologia20213229
  110. 110. KrohmerR. WCrewsD1987Facilitation of courtship behavior in the male red-sided garter snake (Thamnophis sirtalis parietalis) following lesions of the septum or nucleus sphericus.Physiology and Behavior, 40759765
  111. 111. KyleA. LPeterR. E1982Effects of brain lesions on spawning behaviour in the male goldfish. Physiology and Behavior, 2811031109
  112. 112. KyleA. LStaceyN. EPeterR. E1982Ventral telencephalic lesions: Effects on bisexual behavior, activity, and olfation in the male goldfish.Behavioral and Neural Biology36229241
  113. 113. LavioletteS. RLipskiW. JGraceA. A2005A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input.Journal of Neuroscience, 25606675
  114. 114. LeDouxJ. E. (1992Brain mechanisms of emotion and emotional learning.Current Opinion in Neurobiology2191198
  115. 115. LeDouxJ. E. (1995Emotions: Clues from the Brain. Annual Review of Psychology46209235
  116. 116. LeDouxJ. E. (2000Emotion circuits in the brain. Annual Review of Neuroscience, 23155184
  117. 117. LeDouxJ. E. (2012Rethinking the Emotional BrainNeuron73653676
  118. 118. LeDouxJ. E., Sakaguchi, A., Iwata, J. & Reis, D. J. (1986Interruption of projections from medial genicualte nuclesu mediate emotional responses conditioned by acoustic stimuli. Journal of Neuroscience, 4683698
  119. 119. LiX. FStutzmannG. ELeDoux, J. E. (1996Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways.Learning and Memory, 3229242
  120. 120. LiangK. CBennettCMcgaughJ. L1985Peripheral epinephrine modualtes the effects of posttraining amygdala stimulation on memory. Behavioral Brain Research, 1593100
  121. 121. LiangK. CMcgaughJ. L1983Lesion of the stria terminalis attenuate the amnestic effect of amygdaloid stimulation on avoidance responses. Brain Research274309318
  122. 122. LiangK. CMcgaughJ. LMartínezJ. LJensenR. AVázquezB. JMessingR. B1982Posttraining amygdaloid lesions impair retention of an inhibitory avoidance response. Behavioral Brain Research, 4237249
  123. 123. LidskyT. ILevineM. SKreinickC. JSchwartz-baumJ1970Retrograde effects of amygdaloid stimulation on conditioned suppression (CER) in rats.Journal of Comparative and Physiological Psychology73135149
  124. 124. LohmanA. H. MSmeetsW. J. A. J1990The dorsal ventricular ridge and cortex of reptiles in historical and phylogenetic perspective. In B. L. Finlay, G. Innocenti & H. Scheich (Eds.). The neocortex: ontogeny and phylogeny. Plenum Press, New York, 5974
  125. 125. LowndesMDaviesD. C1994The effects of archistriatal lesions on one-trial passive-avoidance learning in the chick.European Journal of Neuroscience, 6525530
  126. 126. LynchGLarsonJStaubliUGrangerR1991Variants of synaptic potentiation and different types of memory operations in hippocampus and related structures. In: L. Squire, N. M. Weinberger, G. Lynchand & J. L. McGaugh (Eds.). Memory: organization and locus of change. Oxford University Press, New York, 330363
  127. 127. MacphailE. M1996Cognitive function in mammals: the evolutionary perspective.Cognitive Brain Research3279290
  128. 128. MadisonD. VMalenkaR. CNicollR. A1991Mechanisms underlying long-term potentiation of synaptic transmission.Annual Review of Neuroscience14379397
  129. 129. Magdaleno-madrigalV. MMartinez-vargasDValdés-cruzAAlmazán-alvaradoSFernández-masR2010Preemptive effect of nucleus of the solitary tract stimulation on amygdaloid kindling in freely moving catsEpilepsia51438444
  130. 130. MajchrzakMFerryBMarchandA. RHerbeauxKSeillierABarbelivienA2006Entorhinal cortex lesions disrupt fear conditioning to background context but spare fear conditioning to a tone in the rat.Hippocampus16114124
  131. 131. MalenkaR. CNicollR. A1993NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms.Trends in Neurociences, 16521527
  132. 132. MarenSAharonovGFanselowM. S1996Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: Absence of a temporal gradiente. Behavioral Neuroscience, 110718726
  133. 133. MarenSFanselowM. S1995Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivoJournal of Neuroscience, 1575487564
  134. 134. Marino-netoJSabbatiniR. M1983Discrete telencephalic lesions accelerate the habituation rate of behavioral arousal responses in Siamese fighting fish (Betta splendens).Brazilian Journal of Medical and Biological Research16271278
  135. 135. Martínez-garcíaFNovejarqueALanuzaE2007Evolution of the amygdala in vertebrates. In: J. H. Kaas (Ed.) Evolution of Nervous Systems, 2The Evolution of Nervous Systems in Non-Mammalian Vertebrates. Academic Press, Oxford, 255334
  136. 136. MaserJ. DKlaraJ. WGallupG. G1973Archistriatal lesions enhance tonic immobility in the chicken (Gallus gallus).Physiology and Behavior, 11729733
  137. 137. McdonaldA. J1992Cell types and intrinsic connections of the amygdala. In: Aggleton, J. P. (Ed). The amygdala: Neurobiological aspects of emotion, memory and mental disfunctions. Wiley-Liss, New York, 6796
  138. 138. McdonoughJ. HKesnerR. P1971Ammesia produced by brief electrical stimulation of the amygdala or dorsal hippocampus in cats. Journal of Comparative and Physiological Psychology, 77171178
  139. 139. McenteeW. JCrookT. H1993Glutamate: its role in learning, memory and aging brain,Psychopharmacology111391401
  140. 140. McgaughJ. LFerryBVazdarjanovaARoozendaalB2000Amygdala: Role in modulation of memory storage. In J. P. Aggleton (Ed.), The amygdala. Oxford University Press, London, England, 391423
  141. 141. McgaughJ. LGoldP. E1974The effects of drugs and electrical stimulation of the brain on memory storage processes. In: R. D. Myers & R. R. Drucker-Colin (Eds.). Neurohumoral coding of brain function. Plenum Press, New York, 189206
  142. 142. McgaughJ. LGoldP. E1976Modulation of memory by electrical stimulation of the brain. In: M. R. Rosenzweigand & E. L. Bennett (Eds.). Neural mechanisms of learning and memory. The MIT Press, Cambridge, Massachusetts.
  143. 143. McintyreMSteinD. G1973Differential effects of one- versus two-stage amygdaloid lesions on activity, exploration, and avoidance behavior in the albino rat. Behavioral Biology, 9451465
  144. 144. MckernanM. GShinnick-gallagherP1997Fear conditioning induces a lasting potentiation of synaptic currents in vitroNature390607611
  145. 145. MedinaLBupeshMAbellánA2011Contribution of genoarchitecture to understanding forebrain evolution and development, with particular emphasis on the amygdalaBrainBehavior and Evolution, 3216236
  146. 146. MedinaLReinerA1995Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. BrainBehavior and Evolution, 46235258
  147. 147. MorenoNGonzálezA2006The common organization of the amygdaloid complex in tetrapods: new concepts base don developmental, hodological ans neurochemical data in anuran amphibians. Progress in neurobiology, 786190
  148. 148. MorenoNGonzálezA2007Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transitionJournal of Anatomy, 211151163
  149. 149. MorganG. C1974aThe early development of the telencephalon of the marine catfish, Galeichtys felis. Journal fur Hirnforsch, 15427447
  150. 150. MorganG. C1974bThe late embryology and maturation of the telencephalon of the catfish, Galeichtys felis. Journal fur Hirnforsch, 15449468
  151. 151. MorrisR. G. MDavisSButcherS. P1989The role of NMDAreceptors in learning and memory. In: C. J. Watkinsand G. L. Collingridge (Eds.). The NMDA receptor. Oxford University Press, Oxford, IRL Pressand.
  152. 152. MowrerO. H1947On the dual nature of learning: A reinterpretation of “conditionning”and “problem-solving”. Harvard Educational Review, 17102150
  153. 153. MullerJCorodimasK. PFridelZLeDoux, J. E. (1997Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to a explicit conditioned stimulus and to contextual stimuli.Behavioral Neuroscience111683691
  154. 154. MurakamiTMoritaYItoH1983Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebasticus marmoratus.Journal of Comparative Neurology, 216115131
  155. 155. NadelL2008The Hippocampus and Context Revisited. In S. J. Y. Mizumori (Ed.). Hippocampal place fields: relevance to learning and memory. Oxford University Press, New York.
  156. 156. NearyT. J1990The pallium of anuran amphibians. En Jones, E. G. & Peters, A. (Eds). Cerebral Cortex, 8AComparative Structure and Evolution of Cerebral Cortex, Part I. Plenum Press, New York.
  157. 157. NearyT. JBruceL1993Comparisons of forebrain groups among tetrapods. Society for Neuroscience Abstracs, 19, 997.
  158. 158. NieuwenhuysRVerrijdtP. W. Y1983Structure and connections of the telencephalon of the teleostfish Xenomystis nigri. II. The area dorsalis. Acta Morphologica Neerlandaise Scand., 21:330
  159. 159. NobleG. K1939Neural basis of social behavior in vertebrates. Collecting Net, 14121124
  160. 160. NobleG. KBorneR1941The effect of forebrain lesions on the sexual and fighting behavior of Betta splendens and other fishes. Anatomical Record (Suppl.), 79, 49.
  161. 161. NorthcuttR. G1981Localization of neurons afferent to the telencephalon in a primitive bony fish, Polypterus palma.Neuroscience Letters, 22219222
  162. 162. NorthcuttR. G1995The forebrain of gnathostomes: in search of a morphotype. BrainBehavior and Evolution, 46275318
  163. 163. NorthcuttR. G2008Forebrain evolution in bony fishes.Brain Research Bulletin75191205
  164. 164. NorthcuttR. GBrafordM. R1980New observations on the organization and evolution of the telencephalon in actinopterygian fishes. In S. O. E. Ebbesson (Ed.) Comparative neurology of the telencephalon. Plenum Press, New York, 4198
  165. 165. NorthcuttR. GKicliterE1980Organization of the amphibian telencephalon. In: S. O. E. Ebbesson (Ed.). Comparative Neurology of the Telencephalon. Plenum Press, New York.
  166. 166. OkaY1980The origin of the centrifugal fibers to the olfactory bulb in the goldfish, Carassius auratus: An experiment study using the fluorescent dye primuline as a retrograde tracer.Brain Research185215225
  167. 167. Olsson, A. & Phelps, E. A. (2007). Social Learning of fear. Nature Neuroscience, 10 10951102
  168. 168. OttersenO. P1982Connections of the amygdala of the rat. IV: corticoamygdaloid and intra- amygdaloid connections as studied with axonal transport of horseradish peroxidase. Journal of Comparative Neurology, 2053048
  169. 169. OvermierJ. BGrossD1974Effects of telencephalic ablation upon nest-building and avoidance behaviors in East African mouth breeding fish, Tilapia mossambica. Behavioral Biology, 12211222
  170. 170. ParentA1986Comparative neurobiology of the basal gangliaWiley. New York.
  171. 171. ParentA. LDubéM. RBrafordM. RNorthcuttR. G1978The organization of monoamine-containing neurons in the brain of the sunfish (Lepomis gibbosus) as revealed by fluorescence microscopy.Journal of Comparative Neurology, 182495516
  172. 172. ParentM. BMcgaughJ. L1994Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training.Brain Research66197103
  173. 173. ParkesS. LWestbrookF2011Role of the basolateral amygdala and NMDA receptors in higher-order conditioned fearReview of Neurocience, 22317333
  174. 174. ParsonsT. COttoT2008Temporary inactivation of dorsal hippocampus attenuates explicitly nonspatial, unimodal, contextual fear conditioningNeurobiology of Learning & Memory, 9026168
  175. 175. PellegrinoL1968Amygdaloid lesions and behavioral inhibition in the rat.Journal of Comparative and Physiological Psychology, 65483491
  176. 176. PessoaLAdolphsR2010Emotion processing and the amygdala: from a ‘low road’ to a ‘many roads’ of evaluating biological significance. Nature Reviews Neuroscience11773782
  177. 177. PhelpsE. AAndersonA. K1997Emotional memory: What does the amygdala do? Current Biology, 7, R311R314.
  178. 178. PhelpsE. ALeDoux, J. E. (2005Contributions of the amygdala to emotion processing : From animal models to human behavior. Neuron, 48175187
  179. 179. PhillipsR. E1964Wildness” in the mallard duck: effects of brain lesions and stimulation on “escape behavior” and reproduction. Journal of Comparative Neurology, 122139155
  180. 180. PhillipsR. E1968Approach-withdrawal behavior of peach-faced lovebirds, Agapornis roseicolis, and its modification by brain lesions.Behaviour31163184
  181. 181. PhillipsR. GLeDoux, J. E. (1992Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.Behavioral Neuroscience10627485
  182. 182. PhillipsR. EYoungrenO. M1968Unilateral kainic acid lesions reveal dominance of right archistriatum in avian fear behavior.Brain Research377216220
  183. 183. PinuelaCNorthcuttR. G1994Immunohistochemical organization of the forebrain in the white sturgeon. Society for Neuroscience Abstracs, 20, 997.
  184. 184. PitkänenAAmaralD. G1991Demonstration of projections from the lateral nucleus to the basal nucleus of the amygdala: a PHA-L study in the monkey.Experimental Brain Research8346570
  185. 185. PitkänenASavanderVLeDoux, J. E. (1997Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala.Trends in NeurosciencesI, 517523
  186. 186. PitkänenAStefanacciLFarbC. RGoG-GLeDoux, J. E. & Amaral, D. G. (1995Intrinsic connections of the rat amygdaloid complex: Projections originating in the basal nucleus.Journal of Comparative Neurology, 356288310
  187. 187. PortavellaMTorresBSalasC2004aAvoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium.The Journal of Neuroscience 2423352342
  188. 188. PortavellaMTorresBSalasCPapiniM. R2004bLesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius Auratus).Neuroscience Letters3627578
  189. 189. PortavellaMVargasJ. P2005Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systemsEuropean Journal of Neuroscience2128002806
  190. 190. PortavellaMVargasJ. PTorresBSalasC2002The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish.Brain Research Bulletin57397399
  191. 191. PriceJ. LAmaralD. G1981An autoradiographic study of the projections of the central nucleus of the monkey amygdalaJournal of Neuroscience, 112421259
  192. 192. QuinteroEDíazEVargasJ. Pde la Casa LG & Lopez JC. (2011Ventral subiculum involvement in latent inhibition context specificityPhysiology and Behavior, 102414420
  193. 193. RabinakC. AMarenS2008Associative structure of fear memory after basolateral amygdala lesions in ratsBehavioral Neuroscience, 122128494
  194. 194. ReinerANorthcuttR. G1992An immunohistochemical study of the telencephalon of the Senegal bichir (Polypterus senegalus).Journal of Comparative Neurology, 319359386
  195. 195. RibbinkA. J1972The behaviour and brain function of the cichild fish Hemihaplochromis philander. Zoologica. Africanis, 72141
  196. 196. RichardsonRTronsonNBaileyG. KParnasA. S2002Extinction of conditioned odor potentiation of startleNeurobiology of Learning & Memory, 78426440
  197. 197. RiolobosA. SGarciaA. I. M1987Open field activity and passive avoidance responses in rats after lesions of the central amygdaloid nucleus by electrocoagulation or ibotenic acid.Physiology and Behavior, 39715720
  198. 198. RoganM. TLeDoux, J. E. (1995LTP is accompanied by commensurate enhancement of auditory-evoked responses in fear conditioning circuit.Neuron15127136
  199. 199. RoganM. TStäubliU. VLeDoux, J. E. (1997Fear conditioning induces associative long-term potentiation in the amygdalaNature390604607
  200. 200. RoozendaalBKoolhaasJ. MBohusB1993The central amygdala is involved in conditioning but not in retention of active and passive shock avoidance in male ratsBehavioral and Neural Biology, 59143149
  201. 201. RoozendaalBMceweenB. SChattarjiS2009Stress, memory and the amygdala. Nature reviews, 10423430
  202. 202. Roozendaal, B., van der Zee, E. A., Hensbroek, R. A., Maat, H. Luiten, P. G., Koolhaas, J. M. & Bohus, B. (1997). Muscarinic acetylcholine receptor immunoreactivity in the amygdala I. Fear-induced plasticity. Neuroscience, 76 7583 .
  203. 203. RosenJ. B2004The neurobiology of conditiones and unconditioned fear: a neurobehavioral system analysis of the amygdala. Behavioral and Cognitive Neuroscience Reviews, 32341
  204. 204. RosenkranzJ. AGraceA. A2002Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning.Nature41728287
  205. 205. RusschenF. TAmaralD. GPriceJ. L1985The afferent connections of the substantia innominata in the monkey, Macaca fascicularis.Journal of Comparative Neurology, 242127
  206. 206. SabatinelliDFortuneE. LLiQSiddiquiA. PKrafftCOliverWBeckSKhublaiJ2011Emotional perception: Meta-analyses of face and natural scene processingNeuroImage5425242533
  207. 207. SahPFaberE. S. LLopez de Armentia, M. & Power, J. (2003The Amygdaloid Complex: Anatomy and Physiology. Physiological Reviews, 83803834
  208. 208. SahPWestbrookR. FLüthiA2008Fear conditioning and long-term potentiation in the amygdalaAnnals of New York Academy of Sciences, 11298895
  209. 209. Sánchez-riolobosA1986Differential effect of chemical lesion and electrocoagualtion of the central amygdaloid nucleus on active avoidance responses. Physiology and Behavior, 36441444
  210. 210. SavageG. E1971Behavioural effects of electrical stimulation of the telencephalon of the goldfish, Carassius auratus.Animal Behaviour19661668
  211. 211. SavanderVGoC. GLeDoux, J. E. & Pitkänen, A. (1995Intrinsic connections of the rat amygdaloid complex: projections originating in the accessory basal nucleus.Journal of Comparative Neurology, 374291313
  212. 212. ScaliaFEbbessonS. O. E1971The central projections of the olfactory bulb in a teleost, (Gymnothorax funebrisBrainBehavior & Evolution, 4376399
  213. 213. SchneiderA. MWilkinsEFirestoneAEverbachE. CNaylorJ. CSimsonP. E2003Enhanced retention in the passive-avoidance task by 5-HT1A receptor blockade is not associated with increased activity of the central nucleus of the amygdalaLearning & Memory, 10394400
  214. 214. SchuhmacherAMössnerRJessenFScheefLBlockWBellocheA. CLennertsLWelperHHöfelsSPfeifferUWagnerMMaierWSchwabSZobelA2012Association of amygdala volumes with cortisol secretion in unipolar depressed patients.Psychiatry research3196103
  215. 215. SegaarJ1961Telencephalon and behavior in Gasterosteus aculeatus. Behaviour, 18256287
  216. 216. SegaarJ1965Behavioural aspects of degeneration and regeneration in fish brain: A comparison with higher vertebrates.Progress in Brain Research14143231
  217. 217. SegaarJNieywenhuysR1963New etho-physiological experiments with male Gasterosteus aculeatus, with anatomical commentAnimal Behaviour11331344
  218. 218. SeldenNR. WEverittB. JJarradL. ERobbinsT. W. (1991Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues.Neuroscience42335350
  219. 219. SeymourBDolanR2008Emotion, decision making, and the amygdala. Neuron, 58662671
  220. 220. SmeetsW. J1990InE. GJonesAPeters (Eds.). Comparative Structure and Evolution of Cerebral Cortex. Plenum Press.
  221. 221. StriedterG. F1991Auditory, electrosensory and mechanosensory lateral line pathways through the forebrain of channel catfishes. Journal of Comparative Neurology, 312311331
  222. 222. StriedterG. F1997The telencephalon of tetrapods in evolution. BrainBehavior and Evolution, 49179213
  223. 223. TakashinaKSaitoHNishiyamaN1995Preferential of avoidance performances in amygdala-lesioned mice. Japanish Journal of Pharmacology, 67107115
  224. 224. TarrR. S1977Role of the amygdala in the intraspecies aggressive behavior of the iguana lizard, Sceloporus occidentalis. Physiology and Behavior, 1811531158
  225. 225. ThatcherR. WKimbleD. P1966Effect of amygdaloid lesions on retention of an avoidance response in overtrained and nonovertrained rats. Psychonomic Science, 6910
  226. 226. The Avian Brain Nomenclature Consortium (2005Nature Review Neuroscience, 6(2), 151-159
  227. 227. TraversoL. MQuinteroEVargasJ. PDe La CasaL. GLópezJ. C2010Taste memory trace disruption by AP5 administration in basolateral amygdala.Neuroreport2199103
  228. 228. UrsinH1965Effect of amygdaloid lesions on avoidance behavior and vision discrimination in cats. Experimental Neurology, 11298317
  229. 229. UrsinHJellestadFCabreraI. G1981The amygdala, exploration and fear. In: Y. Ben-Ari (Ed.). The Amigdaloid Complex. Elsevier, Amsterdam, 317329
  230. 230. Van Der GaagCMinderaaR. BKeysersC2007The BOLD signal in the amygdala does not differentiate between dynamic facial expressionsSocial Cognitive and Affective Neuroscience, 293103
  231. 231. Van Der ZeeE. ARoozendaalBBohusBKoolhaasJ. MLuitenP. G1997Muscarinic acetylcholine receptor immunoreactivity in the amygdala I. Cellular distribution correlated with fear-induced behavior.Neuroscience766373
  232. 232. VargasJ. PLopezJ. CPortavellaM2009What are the functions of fish brain pallium? Brain Research Bulletin, 79436440
  233. 233. VowlesD. MBeasleyL. D1974The neural substrate of emotional behavior in birds. In: I. J. Goodmanand & M. W. Schein (Eds.). Birds: Brain and Behavior. Academic Press, New York.
  234. 234. WalkerD. LPaschallG. YDavisM2005Glutamate receptor antagonist infusions into the basolateral and medial amygdala reveal differential contributions to olfactory vs context fear conditioning and expression.Learning & Memory, 1212029
  235. 235. WerkaTSkarJUrsinH1978Exploration and avoidance in rats with lesions in amygdala and piriform cortex.Journal of Comparative and Physiological Psychology92672681
  236. 236. WhalenP. J1999Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Current Directions in Psychological Science, 7177187
  237. 237. WiersmaAKonsmanJ. PKnollemaSBohusBKoolhaasJ. M1998Differential effects of CHR infusion into the cetral nucleus of the amygdala in the Roman high-avoidance and low-avoidance rats. Psychoneuroendocrinology, 23261274
  238. 238. WilenskyA. ESchafeG. EKristensenM. PLeDoux, J. E. (2006Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning.Journal of Neuroscience, 261238712396
  239. 239. WilenskyA. ESchafeG. ELeDoux, J. E. (2000The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning.Journal of Neuroscience, 2070597066
  240. 240. WiltgenB. JSandersM. JAnagnostarasS. GSageJ. RFanselowM. S2006Context fear learning in the absence of the hippocampus.Journal of Neuroscience, 26548491
  241. 241. WitkinsJ. M1995Role of NMDA receptors in behavior and behavioral effects of drugs. In: T. W. Stone (Ed.). CNS Neurotransmitters and Neuromodulators: Glutamate. CRS Press, Boca Raton, Florida, 323350
  242. 242. WullimanM. F & Rink, E. (2002The teleostean forebrain: A comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization. Brain Research Bulletin, 57363370
  243. 243. ZeierH1971Archistriatal lesions and response inhibition in the pigeon.Brain Research31327339
  244. 244. ZeierHKartenH. J1971The archistriatum of the pigeon: Organization of afferent and efferent connections.Brain Research31313326
  245. 245. ZhuikovA. YCouvillon, PA & Bitterman, ME. (1994Quantitative two-process analysis of avoidance conditioning in goldfish.Journal of Experimental PsychologyAnimal Behaviour Processes, 203243

Written By

Juan Pedro Vargas, Juan Carlos López and Manuel Portavella

Submitted: 14 December 2011 Published: 19 December 2012