Various strategies that were found to enhance neuroplasticity.
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More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
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\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
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Since the creation of Charles Darwin?s theory of evolution [1], most studies in the field of evolutionary neuroscience were focused mainly on the phylogenetic continuity in the evolution of the central nervous system in vertebrates. A central problem of comparative neurobiology was a search for homologous brain structures in different taxa of vertebrates through the identification of common ancestral (plesiomorphic) and acquired (apomorphic) traits (see for references [2, 3, 4]). At the same time remarkable diversity of brain structures in every vertebrate divergent lineage is a result of two evolutionary pathways – phylogenetic history and adaptive specialization (apomorphosis and idioadaptation according to Severtsov [5]). The second pathway is a key in the origin of homoplasy (parallel and convergent evolution). Two non-antagonistic but rather complementary approaches – historical (phylogeny) and causal (evolving adaptive mechanisms) Dobzhansky considered necessary for the evolutionary synthesis [6]. A combination the embryogenetic, morphological, histochemical and functional approaches as well as the introduction of modern molecular and genetic methods led to a partial or even total revision of some classical views of brain evolution. One of the most crucial achievements was the revision of the old concept of the homology between the basal ganglia and isocortex in Sauropsida amniotes and mammals. According to the new concept, a great part of the avian and reptilian telencephalon, previously considered as a homolog of the striatum, has a pallial origin and is homologous to the mammalian cortex. Like in mammals, the basal ganglia (striatopallidum) occupy only the ventral part of the telencephalic hemisphere. On this basis, the nomenclature of telencephalic structures in birds has been modified [7, 8, 9, 10]. Birds were thus rehabilitated as possessors of the highly developed pallium as compared to the telencephalic cortex in mammals. Behavioral studies conducted in various species of birds and reptiles also led to the reevaluation of their cognitive capabilities, in some avian species as compared to those in primates [9, 11, 12, 13]. However, the issues of what parts of the mammalian cortex are homologous to the avian telencephalic pallial parts targeted by the thalamic relаy nuclei still remain a matter of indefatigable debate.
While the homology of the thalamofugal (geniculocortical) pathway in amniotes is now generally accepted, two alternative hypotheses have been advanced regarding the homology of the thalamopallial tectofugal and auditory pathways. According to the “neocortex hypothesis, ” the thalamic projection fields in the pallium of birds and reptiles are homologous to the mammalian isocortex (a dorsal pallium derivative) [7, 8, 10, 14, 15]. The “claustroamygdalar hypothesis” draws a homology between them and a part of the claustroamygdalar complex (a ventral/lateral pallium derivative) [4, 16, 17]. Respectively, thalamic projection nuclei in reptiles and birds are comparable either with dorsothalamic relay nuclei in mammals (“neocortex hypothesis”) [8, 10, 14, 15] or a part of the thalamic complex of intralaminar and posterior nuclei (“claustroamygdalar hypothesis”) [4, 16, 18]. There is no final solution for this problem.
Phylogenetic transformations in the sensory thalamo-telencephalic systems were considered by the classics of comparative neurology as critical for understanding the forebrain evolution. In the laboratory of A.I. Karamian, the visual, auditory and somatosensory systems were investigated for many years (1958–1989) in the wide range representatives of different vertebrate classes. It was established that these systems consist of parallel pathways, having different morphological and functional characteristics, and different rates of phylogenetic development (see Refs. [19, 20, 21, 22]).
We are carrying out comparative studies of the visual and auditory systems in amniotes, and birds (Archosauria), descending from a common ancestor and thus, having a key significance for understanding the forebrain evolution. As new complementary tests, characterizing the organization of the visual and auditory centers, we used: (1) immunohistochemical analysis of expression of parvalbumin (PV) and calbindin (CB), calcium-binding proteins serving as functionally selective neuronal markers and (2) histochemical evaluation of cytochrome oxidase (CO) metabolic activity reflecting the level of neuronal functional activity. Expression of calcium-binding proteins was studied using the standard procedure of immunohistochemistry on free-floating 40 μm sections. Monoclonal mouse anti-PV (Sigma, USA) diluted 1:1000 and polyclonal rabbit anti-CB (Swant, Switzerland) diluted 1:5000 were used. Cytochrome oxidase activity was revealed on free-floating 40 μm sections according to the convenient histochemical method using cytochrome c from bovine heart, type III (Sigma, USA) as well. Sections were observed and analyzed using the microscope Zeiss Axio Imager A1 (Zeiss, Germany). Images were taken from representative sections with the digital camera mounted on the microscope. Digital images were created using Adobe Photoshop 7.0 (Adobe Systems Incorporated, USA) and assembled into montages. General adjustments of color, contrast, and brightness were made.
This chapter offers a brief comparative survey of our previously published and recently obtained results in the thalamic visual and auditory centers in turtles and pigeons, as well as their analysis in the light of the relevant literature data and present knowledge in this field. We set ourselves the task of elucidating: (1) to what extent the patterns of PV and CB immunoreactivity coincide in homologous centers of reptiles and birds; (2) whether the expression of PV and CB correlates with CO activity; and (3) whether these data can shed light on the role of the phylogenetic and functional (adaptive) factors in determining the PV and CB specificity of the sensory centers.
Across all sauropsids (nonarchosaurian reptiles, Archosauria: birds and crocodiles), the visual system includes two main pathways projecting to the telencephalon, tecto- and thalamofugal, that have different properties. Within the tectofugal pathway in reptiles and birds, projections of retinal ganglion cells successively relay in the optic tectum, thalamic nucleus rotundus (Rot), which further projects to the visual dorsolateral region of the anterior dorsal ventricular ridge (ADVRdl) in reptiles and to the entopallium (Ent) in birds. Within the thalamofugal pathway, retinal ganglion cells directly project to the thalamic relay nucleus geniculatus lateralis, pars dorsalis (GLd), which then projects, in reptiles, to the dorsolateral cortex and, in birds, to the hyperpallial Wulst. Homology between these systems in reptiles and birds is generally accepted. They are comparable, according to “neocortex hypothesis, ” to the mammalian thalamo (nucleus lateralis posterior+pulvinar)-extrastriate and geniculo-striate systems, respectively [3, 8, 9, 10].
Our results show that the tectofugal thalamic center Rot has a higher metabolic (CO) activity both in turtles (Figure 1a-c) and pigeons (Figure 1d, f) as compared to the thalamofugal center GLd. This correlates with the leading role of the tectofugal (collothalamic and extralemniscal) visual system in visual behavior [3]. Differences in the level of CO activity between the Rot and GLd are less significant in pigeons, probably due to a more highly developed thalamofugal visual system in birds.
The activity of cytochrome oxidase in visual centers of turtles and pigeons. Rostrocaudal transverse unilateral sections of the thalamus in turtle (a-c) and pigeon (d-f). Note a high CO activity in the rot and a weaker CO activity in the GLd, both in turtle and pigeon. CO—Cytochrome oxidase; Dla—N. Dorsolateralis anterior; Dma—N. Dorsomedialis anterior; Fpl fasciculus prosencephali lateralis; GLd—N. geniculatus Lateralis, pars dorsalis; rot—N. rotundus; Tr—N. triangularis; Tro—Tractus opticus; Trtt—Tractus tectothalamicus. D—Dorsal; and L—lateral sides. Dorsal and lateral sides are the same here and in other figures. Scale bar: 500 μm.
As for the CaBPr immunoreactivity, the Rot in reptiles and birds differs by the distribution, ratio of РV- and СВ-ir neurons, and intensity of their labeling. In the turtle Rot, strongly labeled CB-ir cells prevailed (Figures 2b and 3a), whereas РV-ir cells were less numerous (Figures 2b and 3b). On the contrary, in the pigeon Rot, strongly labeled РV-ir neurons were prevailing, whereas СВ-ir cells exhibited a restricted distribution pattern and mainly weak labeling (Figures 2d and 3c). In the triangular part of the Rot (Tr), strongly labeled РV- and СВ-ir cells were observed to overlap (Figures 2d and 3c, d). According to multiple studies in other reptilian and avian species, a great interspecies variability was found in the number of РV- and СВ-ir neurons, ranging from the mixed content of both types to the existence of only one of them (see for Refs. [23, 24]). At the same time, both in turtles and pigeons, the Rot has an abundant PV innervation (Figure 3d along with a high CO activity (Figure 1a–f). In birds, the tectorotundal pathway contains multiple parallel channels, deriving from different types of tectal neurons [25, 26] and processing different aspects of visual information [27, 28]. We found that tectorotundal projection neurons in birds and reptiles expressed PV and CB [29, 30]. Thus, a heterogeneous distribution of РV and СВ immunoreactivity in the avian and reptilian Rot may relate to different chemospecificity of parallel tectorotundal channels.
Different specificity to parvalbumin and calbindin of rotundo-telencephalic pathways in turtle (a, b) and pigeon (c, d). Schematic drawings of unilateral transverse sections of the brain at the level of the rot (b, d) and telencephalic areas (a, c), receiving projections from the rot. Circles indicate CB-ir neurons, triangles indicate PV-ir neurons (black are for strongly, white are for weakly labeled cells), and dots indicate immunoreactive terminals. Black arrows mark PV-ir input and striped arrows mark CB-ir input. ADVRdl—Dorsolateral anterior dorsal ventricular ridge; CB—Calbindin; cxl—Cortex lateralis; Ent—Entopallium; path—Pallial thickening; PV—Parvalbumin; rot—N. rotundus; Str—Striatum; Tr—N. triangularis; And Tro—Tractus opticus.
Patterns of parvalbumin and calbindin immunoreactivity in the rot and GLd in turtle and pigeon. Microphotographs of unilateral transverse sections of the thalamus in turtle (a, b) and pigeon (c-f)). Note the prevalence of CB-ir (a) and lesser number of PV-ir (b) cells in the turtle rot in contrast to the prevalence of PV-ir (d) and lesser number of CB-ir cells (c) in the pigeon rot. Both in turtle GLd (a, b) and pigeon GLd—DLAmc, DLL (e, f), prevalence of CB-ir cells (a, e) and lesser number of PV-ir cells (b, f). CB—Calbindin; Dla—N. Dorsolateralis anterior; DLAmc—N. Dorsolateralis anterior magnocellularis; DLL—N. Dorsolateralis anterior lateralis, pars lateralis; Dma—N. Dorsomedialis anterior; GLd—N. geniculatus Lateralis, pars dorsalis; PV—Parvalbumin; rot—N. rotundus; Tr—N. triangularis; And Tro—Tractus opticus. Scale bar: 100 μm.
Both in the turtle GLd (Figure 3a, b and the largest GLd subnuclei (DLAmc, DLL) of pigeons (Figure 3e, f), strongly labeled CB-ir neurons prevailed with РV-ir cells being less numerous. The other avian GLd subnuclei were found to contain cells immunoreactive either to both proteins or only to PV, as in the LdOPT [24]. At the same time, both in turtles and pigeons, CO activity in the GLd was lower than in the Rot with an exception for the LdOPT, where it was very high. Similar to the Rot, there is a great interspecies variability in the patterns of РV and СВ immunoreactivity in the GLd of reptiles and birds (see for references [24]).
In turtles, rotundal РV- and СВ-ir neurons project to the ADVRdl (Figure 2a, b); in pigeons, rotundal neuronal projections terminate in the Ent (Figure 2c, d). Geniculate neurons immunoreactive to these proteins project to the dorsolateral cortex in turtles (see details in [23, 31, 32]) and to the Wulst in birds (see Ref. [24]). The density of telencephalic innervation (immunoreactive dotted neuropil) positively correlates with the number of corresponding immunoreactive cells in the projection thalamic nuclei [23, 31, 32].
The prevalence of PV expression in the Rot and CB expression in the GLd in the zebra finch [33, 34] allowed concluding that in birds, the tectofugal system (Rot-Ent) is PV-specific, while the thalamofugal system (GLd-Wulst) is CB-specific. By contrast, in the comparable visual pathways of mammals [34], the distribution of PV and CB is quite opposite: the extrageniculocortical system (LP/Pulv-extrastriate cortex) is CB-specific. However, the data obtained in the zebra finch cannot be transposed to all avian species because there is a great interspecies variability in the pattern of CaBPr immunoreactivity in the centers of the tecto- and thalamofugal pathways (see Ref. [24]). Similar variability exists in the reptilian thalamic centers of the tecto- and thalamofugal systems, being mainly CB-specific in both cases [23, 24, 31, 32, 35]. Thus, the examples of both similarity and dissimilarity in PV and CB immunoreactivity can be found in homologous visual thalamic centers of reptiles and birds. Here, we disregard the expression of other CaBPr, although, for example, calretinin has been demonstrated in the visual and auditory thalamic centers in reptiles and birds [23, 32, 34, 35, 36].
A study of CaBPr in the thalamus of higher mammals (primates) allowed E. Jones [37] to put forward a hypothesis that PV prevails in the phylogenetically younger, highly specialized lemniscal (core) centers, whereas CB is predominant in the phylogenetically older, less specialized structures (matrix), including the extralemniscal regions (belt/shell) of the sensory nuclei. These findings and the data on CaBPr in the brain structures of nonprimate mammals [37, 38, 39], Sauropsida amniotes and anamniote vertebrates (see [24]), led to a conclusion that distribution of different types of PV- and CB-expressing neurons in brain structures depends on the level of phylogenetic development. However, a high variability in the neuronal PV and CB immunoreactivity in the lemniscal parts of the homologous thalamic sensory nuclei in amniotes, including nonprimate mammals, revealed numerous exceptions of the Jones’ concept. Altogether, they have led us to conclude that at every stage of phylogenetic history, the specificity to different СаВРr types depends on the functional factor (see discussion in [24]).
The auditory system in all amniotes contains two parallel pathways such as lemniscal and extralemniscal. Both of them derive from the mesencephalic auditory center, but from its different regions: the lemniscal stems from the core region, while the extralemniscal—from the peripheral belt region. The lemniscal pathway projects to the core (Red+Revm) of the thalamic auditory center nucleus reuniens (Re) in reptiles and to the core (nCe Ov) of the nucleus ovoidalis (Ov) in birds. The extralemniscal pathway projects to the peripheral regions of these nuclei, respectively, to the Revl in reptiles and the Ovl and Ovm in birds. Both pathways have different morphological, neurochemical, and functional characteristics and different targets in the auditory telencephalic regions: the lemniscal—in the core (central area of the ADVRvm in reptiles, L2 in birds), whereas the extralemniscal—in the belt (peripheral area of ADVRvm in reptiles, L1, L3, CMM in birds) [40, 41, 42, 43, 44, 45, 46, 47, 48].
The distribution of PV and CB immunoreactivity as well as CO activity was different in the central and peripheral regions of the thalamic auditory centers in turtles and pigeons, reflecting their core-belt organization. In turtles, the core region (Red+Revm) contains both СВ- and РV-ir cells as well as a neuropil with prevailing CB immunoreactivity (Figure 4b, c), and exhibits high CO activity (Figure 4a). The belt region (Revl) is distinguished by a weak immunoreactivity to both proteins and a low CO activity (Figure 4a–c). The prevalence of CB-ir cells in Red+Revm positively correlates with a high density of CB-ir neuropil in its projection telencephalic field (ADVRvm) that decreased at the border with the ADVRm (Figure 4e). PV immunoreactivity of neuropil in the ADVRvm was far less dense, while CO activity was rather high, but only outside of neuronal clusters (Figure 4d).
Distribution of calbindin and parvalbumin immunoreactivity and CO activity in the thalamic (re) and telencephalic (ADVRvm) auditory centers in turtle. Transverse unilateral sections at the levels of re (a-c) and ADVRvm (d-f)). A, d—CO activity, b, e—CB, c, f—PV immunoreactivity. Note the highest level of both CB and PV immunoreactivity and CO activity in the red+Revm (core of the re) in contrast to the Revl (belt of the re). Compare the ADVRvm both strongly CB-ir (e) and moderately CO-active (d) terminal neuropil with weakly PV-ir neuropil (f). White areas in d—CO-negative cell clusters. ADVR s– Anterior dorsal ventricular ridge; ADVRm—Medial part of ADVR; ADVRvm—Ventromedial part of ADVR; CB—Calbindin; CO—Cytochrome oxidase; Pedd—Pedunculus dorsalis; PV—Parvalbumin; re—N. Reuniens; red—Re dorsalis; Revl—Re ventrolateralis; and Revm—Re ventromedialis. Scale bar: 100 μm.
Pigeons have a more distinct core-belt organization of the thalamic auditory center Ov as compared to the turtle Re. The Ov core region (nCe Ov), like the turtle Red+Revm, contains both СВ- and РV-ir cells and neuropil, but with prevailing PV immunoreactivity. The density of dotted PV-ir neuropil and the degree of cell labeling therein were greater (Figures 5c, d and 6a) than in CB-ir neuropil and its cells (Figures 5e, f and 6b). A high CO activity of neuropil and its cells clearly distinguished the nCe Ov from the peripheral nuclei Ovl and Ovm, where this activity was absent (Figure 5a, b).
Distribution of calbindin and parvalbumin immunoreactivity and CO activity in the thalamic auditory center (Ov) of the pigeon. Transverse unilateral thalamic sections at the level of the Ov. (a, b)—CO activity located only in the nCe Ov (core). (c, d)—Strong PV immunoreactivity located only in the nCe Ov. (e, f)—CB immunoreactivity located in the nCe Ov, Ovl, and Ovm. Note strongly stained PV-ir and weakly stained CB-ir cells in the nCe Ov (core) in contrast to strongly CB-ir cells in Ovl and Ovm (belt), which are morphologically different from CB-ir cells in the nCe Ov. Note also a high level of CB immunoreactivity in the DMP (e). CB—Calbindin; CO—Cytochrome oxidase; DMP—N. Dorsomedialis posterior; nCe OV—N. centralis Ov; Ov—N. Ovoidalis; Ovl—Ov lateralis; Ovm—OV medialis; PV—Parvalbumin; rot—N. rotundus; SPO –– Nucleus semilunaris parovoidalis; and TrOv—Tractus ovoidalis. Scale bars: 100 μm (a, c, e) and 50 μm (b, d, f).
Core-belt organization of the pigeon nucleus ovoidalis. Schematic drawings of transverse sections of the Ov. The core nCe Ov contains both PV-ir (a) and CB-ir (b) cells and dotted neuropil. Note: Strong labeling of PV-ir and weaker labeling of CB-ir cells, high density of PV-ir neuropil, and low density of CB-ir neuropil. Belt Ovl, Ovm, and SPO contain only strongly labeled CB-ir cells and neuropil (b) and devoid of PV-ir cells (a). CB—Calbindin; nCe OV—N. centralis Ov; Ov—N. Ovoidalis; Ovl—Ov lateralis; Ovm—OV medialis; PV—Parvalbumin; SPO –– Nucleus semilunaris parovoidalis; and TrOv—Tractus ovoidalis.
Like in mammals, the ratio and distribution of СВ- and РV-ir neurons in the lemniscal (core) regions of the Re and Ov significantly differ not only across different Sauropsida taxa but also in different species within the same taxonomic group [33, 36, 37, 48, 49]. These interspecies differences relate to peculiarities in the morphofunctional organization of the lemniscal centers in different species, specifically with different localization of brain stem auditory input projections, encoding information about different parameters of sound signaling. Overall, the variability in CaBPr expression in the lemniscal (core) centers is determined by specific mechanisms for processing each auditory modality. Thus, the phenotypic diversity in the CaBPr expression in lemniscal auditory centers may be considered as a result of the complicated interplay between phylogenetic history and ecology-dependent functional specialization with the leading role of the functionally adaptive factor.
In the extralemniscal peripheral Ov regions (Ovl and Ovm) of pigeons, a distinct monospecificity to CB was revealed. These nuclei contained only CB-ir cells and dense CB-ir neuropil (Figures 5e, f and 6b), being completely devoid of PV immunoreactivity (Figures 5c and 6a). At the same time, CB-ir cells were more densely packed, strongly labeled, and exhibited a different morphological type as compared to CB-ir cells in the nCe Ov (Figures 5f and 6b). This feature is typical for the belt Ov regions in all the studied avian species and for some belt nuclei in the mammalian auditory thalamic center (nucleus geniculatus medialis) (see for Ref. [48]). Such a strong similarity indicates a high evolutionary conservatism of the extralemniscal auditory thalamic center. It is determined by the fact that peripheral parts of the auditory centers have multiple connections with many other nonauditory, including limbic centers, which provide the involvement of auditory information in different vital functions of the brain, responsible for feeding, reproductive, communicative, and other behaviors served species survival [43, 44, 46, 50].
In reptiles and birds (Archosauria), the patterns of calcium-binding protein (PV and CB) expression and metabolic (CO) activity have been shown to differ in distinct areas of the visual and auditory thalamic centers related to different parallel channels within the tecto- and thalamofugal visual pathways as well as the lemniscal (core) and extralemniscal (belt) auditory pathways. No unambiguous positive correlation has been found in the thalamic centers between PV immunoreactivity and high CO activity. The level of metabolic activity is likely to depend on the functional significance of the thalamic centers. The remarkable interspecies variability in PV and СВ expression in homologous centers within every phylogenetic lineage appears to result from complicated interrelationships between phylogeny and epigenetic ecology-dependent functional adaptation, reflecting both conservative and plastic traits in their evolutionary development. The patterns of PV and СВ immunoreactivity in the thalamic centers of the reptilian and avian visual and auditory systems provide evidence in favor of their homology with the mammalian dorsothalamic projection nuclei and, accordingly, the homology of their projection pallial areas with the mammalian isocortical sensory zones, supporting thereby the Karten’s isocortical hypothesis [7, 10].
This work was supported by State budget funding according to the assignment by the Russian Federal Agency for Scientific Organizations (FASO Russia) (Neurophysiological mechanisms of functional regulation and their evolution).
Stroke also known as cerebrovascular accidents is the world’s second death-perpetrating disease after cardiovascular diseases [1, 2], and it affects about 13.7 million people annually in the globe [3]. About one third of all strokes translate into fatalities, and another one third constitutes stroke survivors staying with residual disability that accounts as foremost noticeable root of long-term neurological disability in adults [4, 5] and third most common cause of all disabilities globally [6]. Stroke classically depicts a syndrome with sudden onset of acute focal injury of the central nervous system (CNS) of vascular origin that produces focal or global neurological deficit in accordance with affected area of blood supply [7]. Thus, based on the isolated territory of the brain involve, stroke can be cerebral stroke, brainstem stroke, cerebellar stroke, or thalamic stroke, while based on underline cause it can be ischemic stroke (thrombotic, embolic, lacunar, watershed, or cryptogenic) which results from brain vascular occlusion, or hemorrhagic stroke (intraparenchymal or subarachnoid) which is due to blood-related aberrations [8].
Cerebral stroke results in loss of cerebral cortex related functions that manifests as motor impairment [9, 10, 11], sensory impairment [12, 13, 14], cognitive impairment [15, 16, 17], balance impairment [18] among others. The motor function of the cerebral cortex is embedded in the motor cortex (primary motor area, premotor cortex, supplementary motor area, cingulate motor areas) located in the frontal lobe anterior to central sulcus, the motor cortex is responsible for planning, initiation, execution, and regulation of voluntary movement which is achieved through originating descending corticospinal tract and corticobulbar system to the spinal cord and brainstem respectively [19]. Cerebral cortex plays principal role in sensory/perceptual functions by providing meaning to all sensations (except sense of smell) through primary somatosensory cortex in the postcentral gyrus of the parietal lobe, and other primary cortical sensory areas such as auditory cortex in the temporal lobe and visual cortex in the occipital lobe. Cognitive function involves multifaceted domains of cognitive processes including memory, learning, attention, thought, comprehension, perception, language among others [20]. Each of these domains of cognition requires cerebral cortex, illustration can be seen in memory domain where memory acquisition involves sensory cortex, memory retrieval involves prefrontal cortex, and memory storage is distributed throughout the cortex [21]. Balance and coordination of movement involve integrated functioning of both pyramidal and extra-pyramidal systems, and the cerebral cortex is the main principal origin of pyramidal system.
The mechanism of cerebral damage after stroke determines the cerebral stroke impairments, and the mechanism of damage is relative to whether the type of stroke is ischemic or hemorrhagic. Ischemic stroke consists of five distinct pathophysiologic mechanism each of which has distinct time frame; these includes immediate (within minutes) peri-infarct depolarization and excitotoxicity, hours later by neuro-inflammation and oxidative stress, days later by apoptosis [8]. In addition to ischemia related cascade of events aforementioned, hemorrhagic stroke is associated with two additional unique pathophysiologic phases. The primary; acute phase which is due to physical effect of hematoma (mass effect) from the mass accumulated blood, and the secondary; subacute phase termed as cytotoxicity from secondary metabolites of blood components [22, 23, 24].
Recovery to some extent from post stroke impairments observed among stroke survivors was one of the early evidences that led to move away from outdated dogma widely misconceived previously that; there was no possibility for repair or change within the CNS after it had suffered a lesion; and that once there is damage such as stroke that leads to neuronal demise inadvertently, the brain structures and functions are lost forever [25, 26]. It is now well-established fact that CNS repair or change itself but it just that it relatively does not do well enough, and that functional recovery after damage relies on neuroplasticity [27, 28]. Neuroplasticity is life-long natural capability of the CNS to rearrange itself in both molecular form and function in response to new experience or stimulus. Brain plasticity is pivotal to functional recovery after cerebral stroke, and this spontaneous, endogenous and intrinsic capacity of the brain is what restorative rehabilitation approaches for stroke explore, promote and remodel in the right direction to achieve optimal functional recovery after stroke [29, 30].
There is exploding surge among scientists to pay more attention in searching for various therapeutic strategies that can enhance neuroplasticity to augment functional recovery with rehabilitation after stroke [31, 32, 33, 34]. Although this strategy is still in developmental stage but the reasons for this shift in attention are not far-fetched. Firstly, the thrombolytic/thrombectomy clinical treatment available for acute stroke has a very restrictive time window of administration of 4–5 hours of lesion onset [35]. This is in contrast to restorative/rehabilitative interventions that has unlimited therapeutic window of lifelong applicability [36]. Secondly, rehabilitation interventions are still far from sufficiency for optimal and ideal recovery from impairments after stroke [37], as about 50% of stroke survivors still leaves with residual disability and remain functionally dependent despite rehabilitative management [38]. Understanding the mechanisms of cerebral damage and their recovery after cerebral stroke is essential towards development of strategies that harness and enhance neuroplasticity in combination with rehabilitation processes [39]. This paper therefore discusses the mechanism of cerebral damage after stroke as well as elucidates the concept of neuroplasticity as key for recovery following stroke.
In ischemic stroke, irreversible cascade of damage to the brain tissue ensue once the cerebral blood flow (CBF) reduces to less than 12 ml/100 g/min of the normal range of 50–60 ml/100 g/min. Within seconds of this abrupt ischemic insult, neuronal cells in the center of ischemic region termed as ischemic prenumbra undergoes anoxic depolarization due to loss of ATP-dependent ionic pump homeostasis, and they never repolarize [40]. This necrotic core of ischemic prenumbra is enclosed by a zone of relatively lesser impacted tissue termed as ischemic penumbra, which is abridged functionally silent by the reduced blood flow but maintains metabolically active and therefore can repolarize at the expense of further energy consumption [41]. This repetitive depolarization and repolarization of ischemic penumbra are termed peri-infarct depolarization and the important period of time during which this volume of brain tissue is salvageable is referred to as the window of opportunity. The energy failure in the functioning of ATP dependent sodium potassium pump in the ischemic prenumbra results in massive uncontrolled anoxic depolarization that results in opening of voltage-gated calcium channels, mitochondrial dysfunction which further deplete energy required to maintain ion gradient, and abnormally extracellular buildup of excitatory amino acids [42, 43].
Consequently, excitatory glutamate and other excitatory amino acids such as aspartate becomes excessively released, and glutamate hyperexcitation of glutamate N-methyl-D-aspartate (NMDA) receptor, which is arguably the most calcium-influx allowing ionotropic glutamate receptor; results in massive influx of calcium ion (Ca++) into hypoxic neuron. Calcium ion triggers series of cascading events that ultimately lead to neuronal demise through activation of proteolytic enzymes, stimulation of pathogenic genes, lipid peroxidation and free radical generation [44]. For this; glutamate and other excitatory amino acids are cumulatively termed excitotoxins, and their accompanying neuronal damage termed excitotoxicity [45]. Calcium activates key number of disparaging intracellular enzymes such as proteases, kinases, lipases, and endonuclease that not only wildly permits release of cytokines and other mediators that result in the loss of cellular integrity but also orchestrated triggering of intrinsic apoptotic pathway of neuronal death. Specifically, calcium through mobilizing phospholipases hydrolyses membrane bound glycerophospholipids to yield free fatty acids, which enable free radical peroxidation of other membrane bound lipids. Calcium through mobilizing proteases lyses integral structural proteins and activates nitric oxide synthase enzyme that triggers free radical machinery [46].
Prior excitotoxicity activates microglia and astrocytes which are the brain resident innate immunity to reacts and release cytokines, chemokines (chemotaxis cytokines), and matrix metalloproteases (MMPs). This constitutes neuro-inflammation, and microglia activation institutes the initial vital neuro-inflammatory response in acute stroke, which together with blood-borne innate immune cells and later adaptive immune cells support the course. This neuro-inflammatory response supposedly aims to reduce injury processes but this response under stroke pathology develops improperly more reactive and aggressive to yield numerous inflammatory mediators that trigger apoptosis and orchestrate lethal neuronal injury [47, 48]. Activated microglia becomes phagocytes that can release plethora of substances, some of which are neuroprotective such as neurotropic factors; nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), insulin-like growth factor I (IGF-I), and growth associated protein (GAP-43/B-50), while some are neurotoxic such as tumor necrosis alpha (TNF-α), interleukin-1β (IL-1β), and interleukin-6 (IL-6). Blood–brain barrier (BBB) which confers brain with protection against systemic toxins is disrupted by matrix metalloproteinases (MMPs) with MMP-2 (gelatinase A) and MMP-9 (gelatinase B) being the leading concerns in cerebral ischemia [49]. MMP-2 that is normally expressed at low levels becomes increased during cerebral ischemia to galvanizes MMP-9, which abolishes components of the basement membrane in the vascular wall leading to BBB distraction, thus allowing further infiltration of inflammatory mediators and other potential toxins [50].
Oxidative stress signifies disparity in the high-level oxidants (free radicals) with respect to corresponding nonconforming low level of antioxidants. Long term cerebral hypo-perfusion produces abnormal proportions of reactive oxygen species (ROS) and/or reactive nitrogen species (RNS) oxidants through several mechanisms of injury, such as mitochondrial inhibition, calcium ions overload, ischemia–reperfusion injury, and neuroinflammation [51]. During cerebral ischemia, there is mitochondrial inhibition of oxidative phosphorylation due to the lack of sufficient oxygen, and the oxygen depleted cell shift to glycolytic pathway of ATP generation that results in lactate and hydrogen ion (H+) build-up in the mitochondria and the consequent reversal of the H+ uniporter on the mitochondrial membrane that results in superfluous cytosolic H+ buildup and acidosis [52]. Acidosis partly lead to oxidative stress by supplying excessive H+ for the successive progression in the generation of hydrogen peroxide (H2O2) and the final hydroxyl radicals (∙OH) either in the turnout of transition metal ions (Fenton reaction) or in the presence of superoxide radical (Haber-Weiss reaction), with this effect more pronounced in neurons due to inherently low anti-oxidant defense. In addition, the compelling protein and lipid oxidant peroxynitrite (OONO_) of RNS is favorably generated in the oxygen depleted cell by the reaction of nitric oxide (NO) and superoxide (O2∙−), thereby also contributing to oxidative stress.
Calcium overloads, as a result of glutamate mediated NMDA receptor excitotoxicity, also contributes in neuronal oxidative stress at cytosolic and mitochondrial level. At cytosolic level, excessive calcium ion activation of key intracellular enzymes such as neuronal nitric oxide synthase (nNOS) via Ca2+ binds calmodulin to induce subsequent downstream effect, as nNOS catalysis results in generation of nitric oxide (NO) free radical from L-arginine [53, 54]. At the mitochondrial level, excessive calcium ion influx into mitochondrial matrix leads to the inner mitochondrial accumulation of momentous level of Ca2+ via mitochondrial calcium uniporter (MCU) which proliferates disturbance of usual bio-energetic, mitochondrial ROS, and membrane permeability [55].
Apoptosis is a physiological mechanism of cell death through programmed cellular machinery of either extrinsic or intrinsic pathways [56]. Under stroke pathology, neuronal demise by necrosis preponderance in the ischemic prenumbra is marked by excitotoxicity, while additional process of neuronal demise by apoptosis which is more delayed and predominant in the ischemic penumbra occur in a fashion where apoptosis becomes dysregulated [57]. Thus, while the neurons within the core infarct die by immediate necrosis due to insufficient ATP, the penumbra die by ATP requiring process of apoptosis, supporting the established evidence that cellular demise after cerebral ischemia transpires through both necrosis and apoptosis [58]. Multiple pre-existing pathophysiologic mechanisms that can induce apoptosis after cerebral ischemia includes pro- calcium influx, pro-inflammatory cytokines and oxidative stress [59]. Apoptosis can be caspase-dependent or caspase-independent, and the most common is caspase-dependent which is initiated and triggered through distinctively intrinsic (or mitochondrial) pathway or extrinsic (or death receptor) pathway. Both intrinsic and extrinsic pathways share similar terminal phase termed execution phase where caspase 3 leads to the destruction of cellular components and cell death [60].
In hemorrhagic stroke, the mechanism of damage begins with additional process of mass effect from the mass accumulated blood, and cytotoxicity from the secondary metabolites of blood components, in addition to shared common damaging caused by ischemia such as excitotoxicity, neuroinflammation, oxidative/nitrosative stress, and apoptosis. The initial bleed from the cerebral hemorrhage causes immediate physical disruption of the cellular cytoarchitecture of the brain and increases local pressure which can cause compressions, hypothetically disrupting blood flow and principally causing brain herniation [61]. The subsequent expansion of hematoma causes mass effect of hematoma growth leading to further rise in intracranial pressure, brain herniation, and impacted blood flow that is correlated with neurologic deterioration and degraded clinical outcomes. Depending on the dynamic of hematoma expansion (growth), the primary damage ensues within minutes to hours subsequent to the onset of bleeding and is basically due to mechanical damage associated with the mass effect [62].
Secondary injury after cerebral hemorrhage termed as cytotoxicity occurs due to series of events initiated by the prior primary injury mechanism (mass effect), that is specifically due to body response to the hematoma for instance inflammatory response, and from the multiple blood components released from hematoma [61]. The extravasated blood components released from hematoma being implicated to cumulatively imposed cellular toxicity includes; majorly the erythrocytes and plasma proteins, and the damage-associated molecular patterns (DAMPs) which are nucleic acids, extracellular matrix components, proteins, lipid mediators, ATP and uric acid released from necrotic tissues [63]. At the early stage of cytotoxicity, the toxicity of extravasated blood plasma components such as coagulation factors, complement components, and immunoglobulins are known to be the main contributing factor of cellular damage. Subsequently, erythrocytes lysis leads to release of its major intracellular component hemoglobin (Hb), which when metabolize via hemoglobin metabolic pathway release degradation products; heme and iron (Fe). Both Hb and its degradation products are potent cytotoxic chemicals capable of causing death to many brain cells through mechanism of free radical generation with substantial increase oxidative stress and subsequent damage to DNA [62].
The ultimate goal of stroke management is to promote optimal recovery of lost functions and reduce further injury. This recovery depends majorly on brain plasticity; a spontaneous regeneration process that encompasses neural plastic changes in the lesioned hemisphere to reestablish its structural and functional reorganization. Brain plasticity under pathological condition completely differs from plasticity under properly functioning brain. For instance, plasticity in normally functioning brain is a prerequisite basis of learning and memory that involves plastic adaptation such as long-term potentiation (LTP). This is opposed to plastic changes observed using MRI in cerebral stroke pathology, that involves modification in intracortical myelin, augmented neurogenesis, improved spine density in neuronal dendrites and alterations in astrocyte volume [64].
Stroke recovery to certain extent also depends on severity extent of the initial injury deficit as the severity of the damage is inversely related to the prognosis for recovery [65]. But it was also observed that recovery differs even among post stroke patients with similar clinically assessed severity. This apparently stress the recovery role of other brain endogenous survival mechanism such as extent to which collateral circulation bypass to supply blood to the perilesional neurons, angiogenesis, inhibitory neurotransmitters that counteract excitotoxicity, and multiple representations of the same function in different cortical areas [66]. Appropriate rehabilitation and drug treatment that target underline cause of stroke are also critical to recovery after post stroke cerebral damage. Rehabilitation aims to maximize optimum recovery of lost functions as a result of impairments deficit after stroke but overall, brain plasticity underlies recovery promoted by rehabilitation [67, 68, 69].
Recovery from stroke has also been attributed to be dependent on resolution of early local processes in the brain that includes resolve of perilesional edema, re-emergence of circulation within the ischemic penumbra, resolution of remote functional depression of neurological function induced by process of diaschisis [70]. As previously stated stroke recovery majorly depends on brain reorganization process of plasticity which in turn dictates recovery promoted by rehabilitation. Mechanism through which rehabilitation mediates brain plasticity to promote recovery has been studied and explained. Rehabilitation such as physical therapists stroke interventions modifies neurotrophic factor expression in the CNS especially brain derived neurotrophic factor (BDNF), which in turn upon binding with its tyrosine kinase B (TrkB) cognate receptor recruits a cascade of signaling pathways that ultimately mediates activity-associated plasticity of neurons [71, 72]. Activity-associated plasticity signifies a means of functional and structural neuroplasticity that is tailored by the depolarizing behavior of neurons, and the mechanisms governing activity-associated plasticity includes LTP and activity-associated development of corticospinal circuitry among others [72]. Therefore, through brain plasticity after cerebral stroke, reorganization by recruiting cortical or subcortical structures to adopt the function of the injured tissue, reinforcement of remaining synaptic pathways and then creating new connections, recruitment of other pathways that are functionally alike the damaged tissue but anatomically distinct, strengthening of existing but weaker and functionally silent connections, can all be achieved to recover lost cerebral functions [73].
Neuroplasticity is a general term that covers all available processes of neuronal reorganization possible [66], such as neurogenesis, synaptogenesis, dendritic arborization, axonal sprouting, LTP, recruitment of other pathways, reinforcement of functionally silent synapses. Neurogenesis is the process of generating of neurons of neural cell types from precursors neural stem cells and/or neural progenitor cells (NPCs) [74]. Synaptogenesis is a broad term that encompasses the complex process of synaptic contacts formation, maturation and maintenance which form the basis for establishing neural circuits [75]. Dendritic arborization describes a process of neuronal dendrites tree-like branching out to make new synaptic connection through mechanisms of dendrite morphogenesis [76]. Sprouting is a form of plastic changes in the synapses in which there is axonal synaptic reorganization to modify the efficacy of synapses [77]. LTP is the fundamental form of synaptic plasticity where synapses become strengthened and this forms the cellular basis of learning and memory [78].
Neuroplasticity is regulated by the corresponding cascade of intracellular events that translates into plastic changes. However, the plastic changes may either be adaptive, where it is related with an upsurge in function or maladaptive where it is linked with adverse consequences such as loss of function or augmented damage [79, 80]. This brings about the concept that not all plasticity effect positively on clinical status, that maladaptive plastic changes from dysregulated neuroplasticity result in an aberrant neural organization [79]. Typical example of situation where neuroplasticity becomes maladaptive can be seen in new onset of seizures after long period of cerebral trauma, where aberrant progressive plastic changes in the brain in the form of inappropriate synaptogenesis and axonal sprouting accounts for this late development. Neuroplasticity can also be seen as structural where the plastic changes involves the organization and number of synapses such as synaptogenesis, axonal sprouting and dendritic arborization, or functional where the plastic changes involves the efficacy and strength of synaptic connections such as LTP.
The basis of plastic changes that allows for neuroplasticity to become realistic depend upon factors such as neuronal excitability, which define the ability of a nerve to produce an action potential and in turn depends on the permeability, electrical and chemical state of the neuron [81]. This is then followed by adaptive changes termed plasticity, in which there are stable functional transformations that occur in specific neuronal systems as a result of specific stimuli or the combination of stimuli [82]. Furthermore, it has been revealed that effective and repeated action potentials are required from the presynaptic neuron to stimulate the postsynaptic to cause a change in the strength of an interneuron connection [83]. Cumulatively, the aforementioned process leads to biochemical changes, and anatomical adaptations which reinforce the connections between neighboring neurons, thus accounting for molecular, cellular, systems, and behavioral perspectives of explaining neuroplasticity [84].
The strength of the excitation impulse must exceed the threshold value to increase the synaptic efficacy and the stability of the connections between neurons. Nevertheless, when neurons are stimulated only with subthreshold stimuli, the overall activity of the synapse may decrease [85]. Studies conducted on unilateral lesion of the hippocampus results in the formation of new synapses (synaptogenesis) by the axons from the remaining contra-lateral hippocampal system [86]. Thus, the postsynaptic portion of a synapse continues to function properly despite the degeneration of the presynaptic region, and the surviving axons form new synapses. The fibers that form the (new) synapses are homologous to the damaged synapses, which may significantly facilitate the restoration of normal function.
Table 1 summarized various strategies that were found to enhance neuroplasticity and the mechanism through which modulate neuroplasticity.
Strategy | Proposed mechanism reported to modulate and promote neuroplasticity | References |
---|---|---|
Transcranial direct current stimulation (noninvasive) | Modification of neuronal membrane potentials, consequently persuading neuronal excitability which form part of the basis of neuroplasticity. | [87, 88] |
Deep brain stimulation (invasive) | This by stimulating neuronal network connected to the stimulated region, the pathological neuronal network becomes altered by changes in the neurochemical components thereby inducing morphological changes in both the dendrites (dendritic arborization) and axons (axonal sprouting). | [89] |
Functional Electrical Stimulation (FES noninvasive) | Hypothesized to modulate neuroplasticity through repeated generation of neurons synaptic activity that might facilitate synaptic remodeling, leading to neural reorganization. | [90] |
Aerobic Exercise | Aerobic exercise is linked with surge in neurogenesis and angiogenesis, together with rise in neurotrophic molecules especially BDNF and other growth factors implicated in neurite outgrowth and synaptic plasticity | [91, 92] |
Brain-derived neurotropic factor (BDNF) therapy | By binding of BDNF to its TrkB cognate receptor, two distinctive intracellular signaling pathways namely phosphatidylinositol 3-kinase (PI3K)/Akt and mitogen-activated protein kinase/extracellular-signal-regulated kinase (MAPK/ERK) becomes initiated, thereby regulating transcriptional gene activity of neurite outgrowth and neurogenesis. | [93, 94] |
Statins | Proposed mechanism by which statins modulates neuroplasticity involves indirect effect through statin-mediated increase in proteins such as endothelial nitric oxide synthase (eNOS), vascular endothelial growth factor (VEGF), tissue plasminogen activator (tPA), and brain-derived neurotropic factor (BDNF) among others. | [95] |
Erythropoietin (EPO) therapy | EPO and EPO receptor (EPOR) that both becomes upregulated in response to cerebral ischemia, when supplemented act to indirectly augment neurogenesis through EPO-mediated increase in the expression vascular endothelial growth factor (VEGF) and brain-derived neurotropic factor (BDNF). | [96] |
Phosphodiesterase type 5 inhibitors (PDE-5 inhibitors) | PDE-5 inhibitors competitively inhibit phosphodiesterase enzymes responsible for converting cyclic guanylyl monophosphate (cGMP) back to GMP, thus fostering cGMP accumulation which has diverse cellular effect in the brain including angiogenesis, and neurogenesis which are requirements of neuroplasticity | [97] |
Vascular endothelial growth factor (VEGF) therapy. | Proposed mechanism through which VEGF modulates neuroplasticity involves mediating the PI3K–AKT–nuclear factor kappa B signaling pathway; an intracellular pathway that regulate transcriptional factors involves in neurogenesis | [98, 99] |
Various strategies that were found to enhance neuroplasticity.
Advancement in the understanding of mechanism of cerebral damage after stroke and brain neuroplasticity have continue to be a cutting-edge landmark information towards reducing human disability as a result of stroke. Strategies aimed at harnessing and augmenting neuroplasticity in complement with neurorehabilitation offers reasonable level of hope to maximize stroke recovery and diminish cerebral stroke induced neurological impairments. Although these strategies are rapidly evolving towards achieving clinical viability and success, more is needed to be done especially pertaining to outcome measures of neuroplasticity that rely on biomarkers of neuroplasticity rather than functional or behavioral outcome.
The authors declare no conflict of interest.
IntechOpen's Authorship Policy is based on ICMJE criteria for authorship. An Author, one must:
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