Appearance of immunopositive reactions to neural proteins in the developing human pancreas.
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His fields of interest are intensive cardiac care, CPR, post-cardiac arrest care, device therapy of arrhythmias, defibrillator waveform, and AED development.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"201263",title:"Dr.",name:"Endre",middleName:null,surname:"Zima",slug:"endre-zima",fullName:"Endre Zima",profilePictureURL:"https://mts.intechopen.com/storage/users/201263/images/system/201263.jpg",biography:"Prof. Dr. Endre Zima works as the chief of Cardiac ICU at Semmelweis University Heart and Vascular Center. Dr. Zima is specialized in anesthesiology-intensive care and cardiology. He has authored 13 book chapters and more than 130 journal papers, achieved a Hirsch-index of 14, g-index of 22, and more than 650 independent citations. \nHe has been holding graduate and postraduate lectures and practices in anesthesiology since 2006, and in cardiology since 2008. He is a PhD Lecturer in Semmelweis University since 2010. He obtains an accreditation of EHRA on Cardiac Pacing and Implantable Cardioverter Defibrillators, he is accredited AALS Instructor of European Resuscitation Council. \nHe is a Fellow of the European Society of Cardiology, member of the European Heart Rhythm Association and Acute Cardiovascular Care Association, board member of the Hungarian Society of Cardiology (HSC), president of Working Group (WG) on Cardiac Pacing of HSC , board member of WG of Heart Failure. Dr. Zima is also a member the Hungarian Society of Resuscitation, Hungarian Society of Anesthesiology. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"61446",title:"Development of Human Pancreatic Innervation",doi:"10.5772/intechopen.77089",slug:"development-of-human-pancreatic-innervation",body:'The pancreas of most vertebrates is an organ that combines both endocrine and exocrine functions. Functions of the exocrine pancreas are the synthesis, accumulation and secretion of digestive enzymes (protease, amylase, lipase and nucleases) and preferment (elastase, procarboxypeptidase, trypsinogen, pepsinogen, deoxyribonuclease and ribonuclease). The main function of the endocrine pancreas is regulation of carbohydrate metabolism. Specialised endocrine cells are grouped in units called pancreatic islets or islets of Langerhans. Islets of mammals (including humans) contain four major types of endocrine cells: beta cells secreting insulin, alpha cells secreting glucagon, delta cells secreting somatostatin and PP cells that synthesise pancreatic polypeptide [1]. Recently, another type of pancreatic endocrine cells was described—ghrelin-containing cells (epsilon cells) [2]. Pancreatic innervation is of interest due to its role in the pathogenesis of some diseases including chronic pancreatitis, pancreatic cancer and type 1 diabetes. Pain is the dominant clinical symptom in the majority of cases (73–93%) in patients with pancreatic cancer and pancreatitis. At the same time, the aetiology and pathogenesis of pain in chronic pancreatitis and pancreatic cancer are still unclear and are the subject of numerous studies [3].
In experiments on rodents (mice and rats) and cell cultures, it was indicated that nerve fibres and glial cells located in pancreatic islets may be the first target of autoimmune attack in type 1 diabetes [4, 5, 6, 7]. Recently, there were reports of involvement of the peripheral nervous system in the pathogenesis of types 1 and 2 diabetes in humans [8, 9]. Moreover, the participation of the nervous system in the regulation of maturation, level of proliferation and number of insulin-producing beta cells, both in prenatal pancreatic development and in the postnatal period, was indicated in a number of experimental studies. Therefore, detailed information about the innervation of the endocrine pancreas is needed for understanding the mechanisms of beta cell pool renewal.
The pancreas is well innervated by the autonomic nervous system in various mammalian species [3, 10, 11, 12, 13, 14, 15]. Rich innervation of the blood vessels and the exocrine part of the pancreas as well a more abundant innervation of the islets compared with the surrounding acinar part was detected already in the early studies [16, 17].
Connections between neurons are usually studied using anterograde and retrograde labelling of pathways. Pancreatic innervation was studied in various animal species using different tracing methods involving viruses, cholera toxin B, horseradish peroxidase, True Blue or DiI. It is believed that nerve fibres enter (and exit) in the pancreas as a part of neurovascular trunks. Within the pancreas, they also pass along the blood vessels and terminate (or, conversely, begin) near to the capillary wall and endocrine cells [18]. At the same time, they do not form classical synapses with target cells, but release neurotransmitters into the intercellular space, thus affecting more than one target simultaneously (i.e. they are enpassant synapses) [14]. Using retrograde labelling, the connection of pancreatic innervation with the central parasympathetic and sympathetic neurons in the brain stem, midbrain, hypothalamus and forebrain was shown [19, 20, 21]. Some of these brain centres are involved in monitoring of food intake or circadian rhythms, and it would be logical to assume that they send signals to the pancreas to adapt the digestive ferments and pancreatic hormone secretion to behavioural status. However, the central regulation of these processes has not yet been sufficiently studied [14].
In the pancreas, nerve endings were shown around blood vessels, as well as pancreatic acinar, ductal and endocrine cells, using immunohistochemistry and electron microscopy [17, 18]. Four types of plexuses (perivascular, periductal, periacinar and peri-insular) have been identified in the mouse pancreas [18]. Similar data were obtained in studies on the pancreas of the rat and nutria [22, 23]. One of the most interesting features of the mammalian pancreas is that endocrine cells may form highly organised complexes with structures of the nervous system, so-called neuro-insular complexes (NICs). The structure of NIC in the human pancreas has not been studied in detail since their first description by van Campenhout [24] and Simard [25]. Fujita described two types of NIC, which he observed in the foetal and adult pancreas of the dog, cat and rabbit [26]. Some of the pancreatic ganglia contained endocrine cells forming NIC type I (NIC I). In NIC type II (NIC II), endocrine cells lie on the surface of, or even in the midst of, the nerve bundle. However, the distinction between these two types of complexes is conditional because there is an intermediate type of complex in which islets associate with nerve cells and nerve fibres simultaneously. Thus, in the pancreas, endocrine islets are closely associated with a dispersed neural network, which consists of autonomic nerves including sympathetic, parasympathetic and sensory nerves. Unfortunately, because of depth limitations in microscopy, this network cannot be easily portrayed by standard microtome-based two-dimensional (2D) histology. The systematic development of three-dimensional (3D) islet neurohistology has provided insight into neural-islet regulatory mechanisms and the role of neural tissue remodelling in the development of diabetes [27, 28, 29].
In addition, endocrine cells of pancreatic islets are similar to nervous cells in some biochemical and physiological characteristics. Some proteins expressed in endocrine cells of pancreatic islets are also specific to the nervous system: S100, GFAP (glial fibrillary acidic protein), GAD (glutamic acid decarboxylase), TH (tyrosine hydroxylase), NPY (neuropeptide Y), NSE (neuron-specific enolase) and others [6, 7, 30, 31, 32]. Moreover, a number of transcription factors that are characteristic of the nervous system, such as Ngn3 (neurogenin3), BETA2/NEUROD, etc., are expressed during the differentiation of pancreatic endocrine cells [33, 34, 35]. The cells of the endocrine pancreas are classified as cells of a dispersed (diffuse) endocrine epithelial system. The cells of the dispersed endocrine system are a part of the so-called APUD (amine precursor uptake and decarboxylation) system [36]. These cells have the combined ability to the capture and deposit amine precursors and synthesise biogenic amines. The obvious similarity between the pancreatic endocrine cells and nerve tissue leaves the issue of its causes open to discuss.
The precise innervation patterns of islets are unknown, particularly in humans [37]. Every year reviews are published, in which morphology and function of pancreatic innervation are discussed (see for review [10, 11, 14, 15, 38, 39, 40]). However, the nature and distribution of the nervous system structures in the pancreas were studied mainly in rodents. Interspecies differences in the structure and innervation of the pancreas between humans and experimental animals (mice and rats) are quite large. In humans, the pancreas is a compact organ, while in rodents it is treelike, distributed over the mesentery of the small intestine. Therefore, it is impossible to automatically transfer the data obtained on experimental animals to humans.
In addition, knowledge about the dynamics of innervation during ontogenesis and in various diseases of the pancreas is very limited. Single studies are devoted to the formation of innervation in prenatal human development (mainly in the last century, without the use of modern methods). Therefore, the fine details of pancreatic innervation (such as the distribution of sympathetic and parasympathetic fibres and the formation of neuro-insular complexes) in human ontogenesis are insufficiently studied. This is mainly due to the inaccessibility of the material and to a number of technical difficulties, including the quality of pancreatic autopsy samples due to the activity of enzymes of the exocrine part [40].
However, over the past 10 years, different groups of researchers have made significant progress in the study of the peculiarities of innervation in rodents. The most attention was paid to the influence of the nervous system on the endocrine pancreas. It has been shown that both sympathetic and parasympathetic nervous systems affect postnatal development of the endocrine pancreas and its plasticity in adult animals [9, 41]. For example, after vagotomy there was a decrease in insulin-containing cell proliferation in mice and rats [42]. The important role of the sympathetic innervation for the formation of islet cytoarchitecture and their functional maturation during development was also shown [43].
Thanks to recent progresses in the field of islet research (including the study of isolated islets, in thick slices and in vivo), a number of issues concerning the structure and functions of pancreatic innervation have been clarified (see, e.g. [44, 45, 46, 47]). In this chapter, we summarise the literature data and our previous results concerning the morphological organisation of autonomic innervation in the human foetal and adult pancreas. We also discuss the possible role of the close integration between the nervous system and epithelial and endocrine cells in the development of the endocrine pancreas.
The pancreas is innervated by sympathetic and parasympathetic nerve fibres [11, 13]. The literature data indicate poor innervation of adult human pancreatic islets in comparison with rodents [44, 48, 49, 50]. At the end of the twentieth century, pancreatic innervation by postganglionic adrenergic and cholinergic fibres was intensively studied (for references, see [51]). Single nerve cells and nerve ganglia, both myelinated and unmyelinated nerve fibres of various diameters, have been detected in the human pancreas [23, 37, 48, 49]. In a simplified form, it can be considered that pancreatic sympathetic innervation is effected by the fibres of the ventral trunk and the parasympathetic innervation by the vagus nerve.
Bodies of neurons, which form the efferent preganglionic sympathetic nerve fibres, are localised in the thoracic and upper lumbar segments of the spinal cord (T5–L1) [37, 52] or, according to some literature, in C8–L3 [21, 53]. Myelinated axons of these cells leave the ventral roots of the spinal cord and terminate on the bodies of neurons that lie in the ganglia of the paravertebral sympathetic chain, or pass through this chain via the n. splanchnicus to the celiac (celiac) and superior mesenteric (mesenteric) ganglia, and then terminate on neurons localised in these ganglia [54, 55]. The preganglionic fibres of the sympathetic system secrete acetylcholine (Ach). Postganglionic nerve fibres go to the pancreas, where they secrete norepinephrine, which binds to α and β adrenergic receptors and the neuropeptides galanin and NPY (neuropeptide Y) [10, 11, 53, 56].
In humans, the body and tail of the pancreas are innervated by nerve fibres originating from the ventral plexus and accompanying two arteries: the splenic artery and the transverse artery of the pancreas. The pancreatic head receives the largest number of nerve fibres [57, 58].
In the exocrine pancreas, sympathetic axons contact mostly with intrapancreatic ganglia, blood vessels and ducts. In mice, the innervation of the exocrine part is less pronounced than in humans. The major nerves run along the interlobular arteries and form the peri-insular plexus [18]. At the same time, in mice axons of sympathetic nerves contact alpha cells, while contact with beta cells is not found [44]. The axons of sympathetic nerves also innervate smooth muscle cells and pericytes of blood vessels and perivascular space, forming the so-called sympathetic neurovascular complex. In humans, sympathetic fibres innervate smooth muscle cells and pericytes and rarely contact directly with the endocrine cells. Apparently, the effects of the sympathetic innervation are likely mediated through indirect effects on local blood flow within the islet microcirculation [44, 59].
The bodies of the neurons forming the parasympathetic preganglionic nerve fibres lie in the dorsal motor nucleus of the n. vagus (X) [60, 61, 62] and, possibly, in the nucleus ambiguus [11, 12, 13]. Both of these nuclei are under the control of the hypothalamus. Preganglionic parasympathetic fibres are directed to the pancreas as a part of the vagus nerve branches. In the pancreas, parasympathetic fibres terminate on the bodies of parasympathetic neurons lying in intrapancreatic ganglia [38, 63]. These ganglia contain from 3 to 30 neurons and are usually located in intralobular connective tissue, within lobules or in close proximity to islets [13, 27, 29]. It is also important that these ganglia receive input not only from the parasympathetic nervous system but also from the sympathetic nervous system, as well as fibres from other intrapancreatic ganglia and also from the myenteric plexus [13]. Parasympathetic fibres are also involved in the formation of nerve plexuses around the arteries and mingle with sympathetic fibres.
Preganglionic parasympathetic fibres secrete acetylcholine (Ach), which binds to nicotine receptors on the membranes of neurons [53]. Short, unmyelinated postganglionic fibres terminate on the epithelial cells of acini and ducts, smooth muscle cells and islet cells. Postganglionic parasympathetic fibres release several neurotransmitters (Ach (acetylcholine) and NO (nitric oxide)) and neuropeptides (VIP (vasoactive intestinal peptide), GRP (gastrin-releasing peptide) and PACAP (pituitary-activating adenyl cyclase polypeptide)) [10, 11, 13, 56]. Postganglionic nerve fibres perform their functions mainly via Ach by binding to muscarinic receptors found, in particular, in the endocrine cells of the islets [12, 53]. In mice, postganglionic parasympathetic nerve fibres innervate all types of islets cells [10, 11, 44]. Recently, it was found that parasympathetic islet innervation in humans differs from that in mice: first, it was shown that only a small number of fibres penetrate inside the islets (most of the axons terminate in the exocrine part of the pancreas) [44], and, secondly, it was recently shown that stimulation with Ach mostly stimulates beta and delta cells, whereas alpha cells react to a lesser extent [64]. Interestingly, alpha cells themselves may be the primary source of Ach in human islets [45]. Apparently, in human islets, this classical neurotransmitter regulates the activity of other cell types in a paracrine manner. However, now, this concept is again under revision thanks recently to the work of Tang et al. [29].
In the pancreas, there are afferent (sensory) nerve fibres in addition to efferent sympathetic and parasympathetic innervation [10, 11, 12, 53, 54]. Bundles of sensory nerve fibres leave the pancreas and follow the sympathetic (n. splanchnicus) and vagus nerves. The bodies of sensory sympathetic neurons are localised in the ganglia of the dorsal roots in the spinal cord, mainly at the level of the lower thoracic segments (the so-called spinal afferents) projected on interneuron plates I and IV [52, 65]. For the parasympathetic system, the bodies of afferent neurons are localised in the ganglion nodosum, sending information to the nucleus of tractus solitarii [12, 54]. The neurotransmitters of the sensory nerve fibres are CGRP (calcitonin gene-related peptide) and SP (substance P). Most sympathetic and parasympathetic afferent nerves are sensitive to capsaicin [14]. Capsaicin (vanillin) receptors mainly transmit pain information [66]. In addition, Pacinian corpuscles were described in the pancreas of various mammalian species. The suggested function of this receptor is to transmit information about pressure and vibration stimuli. In the human pancreas, they were discovered in the early twentieth century [67]. Despite this fact being presented in many histology textbooks, in the modern literature, only three cases of these findings (all in pancreatic cancer) were described [67, 68]. In our research, we have studied pancreatic autopsies of 42 foetuses and neonates aged from the 10th to 40th week of gestation and of 65 adults, 18 of whom suffered from diabetes mellitus type 2. In total, more than 1000 sections were investigated. However, Pacinian corpuscles are a rare finding in the human pancreas: we were able to detect Pacinian corpuscles only in one pancreatic section of a newborn with diagnosed diabetic fetopathy. Thus, Pacinian corpuscles do not appear to play a significant role in the sensory innervation of the human pancreas.
In some studies on pancreatic innervation, it is assumed that the pancreas is innervated not only by extrinsic efferent and afferent nerves but also by intrinsic enteric neurons of the so-called enteric nervous system (ENS) [12, 69]. The ENS controls the motor, secretion and other functions of the gastrointestinal tract and is closely related with the diffuse endocrine system [70]. Enteric ganglia have some morphological and functional differences from sympathetic and parasympathetic ganglia:
The ENS performs complex integrative functions independently of higher nerve centres.
In the ENS, a large number of various neurotransmitters, many of which are characteristic of the central nervous system, are produce.
Unlike other autonomous ganglia, enteric ganglia do not contain connective tissue and blood vessels. Enteric ganglia are demarcated from the surrounding tissue of the so-called blood-ganglionic barrier, similar to the blood–brain barrier. It is insufficiently studied, and not all researchers agree with its existence.
Glial cells of enteric ganglia are similar in morphology, cell markers and functions with astrocytes of the CNS.
The complex structure of the enteric nervous system, containing a variety of morphological and functional types of neurons and their neurotransmitters, allows the ENS to perform complex reflex acts, some of which are implemented autonomously and some in interaction with the central nervous system and other parts of the autonomous nervous system. Intrapancreatic ganglia are connected with autonomous ganglia in the intestinal nerve plexus [71, 72, 73]. Neurotransmitters for neurons of these ganglia are, among others, serotonin and nitric oxide (NO) [73]. However, according the dominant viewpoint, intramural pancreatic neurons belong to the parasympathetic system.
As was mentioned earlier, the pancreas combines exo- and endocrine functions, secreting digestive enzymes and hormones, which regulate glucose homeostasis. The nervous system regulates the activity of both the endocrine and exocrine pancreas. However, it is problematic to separate the innervation of the pancreatic endocrine part from the innervation of the exocrine, since the tracing method used for this purpose belongs to the pancreas as a whole. In addition, the activity of both endocrine and exocrine parts of the pancreas depends on food intake. Therefore, it is not surprising that the cephalic phase has been described for both pancreatic parts. Although the stimulation of the ventromedial hypothalamus and efferent sympathetic and parasympathetic neurons affects the secretion of islet hormones (see below), it is unknown whether this stimulation is direct through axons innervating the islet or indirect by activating other organs, which affect insulin and glucagon secretion [14]. Moreover, it is very difficult to separate the nervous system effects from other (e.g. humoral) influences.
So, in the laboratory of I.P. Pavlov, in 1895, I.L. Dolinsky conducted an experiment in which he established that acid injection into the duodenum causes a release of pancreatic juice [74]. In 1901, British physiologists William Baileys and Ernest Starling concluded that there is some substance released by the duodenum that stimulates secretion by the pancreas. In the following year, 1902, this substance was discovered and named secretin. Secretin was the first such “chemical messenger” identified. This type of substance is now called a hormone.
At the same time, in the classic studies of I. P. Pavlov with M. A. Afanasiev, the nervous mechanism of pancreatic secretion was found. In the work “On secretory nerves of the pancreas” (1877), they showed that vagus nerve stimulation causes pancreatic secretion. Moreover, I. P. Pavlov with his colleagues detected that imaginary feeding in animals with chronic pancreatic fistula causes an abundant release of pancreatic juice. Later, this was confirmed by the studies of K. M. Bykov and G. M. Davydov in patients with pancreatic fistula. An abundant pancreatic juice released by this patient occurred while talking about delicious food [74]. However, pancreatic juice obtained after vagus nerve stimulation is released in a small quantity and is rich in proteins and enzymes, whereas after the secretin injection, it contains little proteins and enzymes and is released in large quantities [74]. It should be noted that both these factors (nervous and humoral) act simultaneously and synergistically.
Currently, it is considered that efferent sympathetic nerve fibres indirectly inhibit the release of enzymes of the exocrine pancreas by suppressing the stimulating effects of ganglia and constriction of vessels (vasoconstriction), thereby reducing blood flow [13, 59]. The stimulation of short, unmyelinated postganglionic parasympathetic fibres increases release from secretory cells of the exocrine pancreas and ducts causing vasodilation [13, 57].
The autonomous nervous system also regulates hormone release in the endocrine pancreas, thereby affecting glucose metabolism [10, 11, 14, 53]. Many various chemical factors affect insulin and glucagon expression. Auto-, juxta-, para- and endocrine ways potentially regulate secretion of islet hormones. Since the classical studies of Claude Bernard, which showed that injection into the floor of the fourth ventricle causes hyperglycemia, the involvement of the nervous system in the regulation of pancreatic endocrine function and metabolic control has been shown in many studies. It is, therefore, rather difficult to separate one effect from the other [14, 53].
The cellular architecture of islets affects paracrine regulation and synchronises the release of insulin [75]. All pancreatic islets secrete hormones consistently, with an approximately 5-min interval [76]. In order to create this secretion pattern, the activity of insulin-containing beta cells must be consistent both within the individual islet and between the islets [14]. At the same time, the secretory activity of other islets endocrine cells, such as glucagon-secreting alpha cells that have opposite effects on glucose homeostasis, should be consistent with the activity of beta cells. Thanks to this interaction, endocrine cells can simultaneously send signals regulating the effective delivery of islet hormones into the circulatory system and, ultimately, to the liver, regulating the maintenance of glucose homeostasis [76].
However, the islets of Langerhans are a part of a complex coherent system. They are also exposed to humoral factors such as circulating plasma hormones (e.g. epinephrine). The brain also regulates the secretion of islet hormones via the autonomic nervous system [14]. Thus, in works by Akmaev et al. [19], it was shown that the hypothalamus is able to stimulate insulin secretion from beta cells of pancreatic islets along the nerve pathway, which was named “paraventricular-vagal.” This pathway starts from small neurons of the paraventricular nucleus (PVN) of the hypothalamus, synaptically switches in the medulla oblongata to neurons of the dorsal nucleus of the vagus nerve and reaches the pancreatic islets in the composition of the vagus nerve. In this pathway, beta cells receive stimulating signals. Inhibitory signals come from neurons by a humoral way: PVN neurons secrete corticotropin-releasing hormone, which stimulates the secretion of adrenocorticotropic hormone in the pituitary gland that induces the secretion of glucocorticoids in the adrenal cortex. Glucocorticoids inhibit insulin release from beta cells. This kind of double control, according to the authors, is typical for the regulation of endocrine functions. Recently, there has been data that significantly complements this concept: various areas of the hypothalamus have different effects on the secretion of insulin and/or glucagon [77]. So, a detailed study of this system is needed to further identify both neurons and functionally related projections of the central nervous system regulating islet functions.
For most species studied, it is characteristic that nerve fibres are localised mainly at the periphery of the pancreatic islets, forming a peri-insular nervous network [17]. Only single nerve fibres are detected within islets. The bodies of ganglion neurons are also rarely localised in the pancreatic islets and may be in direct contact with endocrine cells [17, 27, 29, 78, 79].
It is believed that autonomic innervations indirectly affect the release of insulin in the cephalic phase during food intake and also take part in the increase of glucagon and decrease of insulin release by sympathetic stimulation [10, 80]. Stimulation of the splanchnic nerve increases the release of glucagon and reduces the release of insulin and somatostatin from endocrine cells of the pancreas [12, 14, 15]. Sympathetic nerves are also believed to be involved in islet response for hypoglycemia, which includes increased glucagon secretion and inhibition of insulin secretion. The general sympathetic effect is expressed by reducing the insulin concentration in plasma (by increasing the concentration of catecholamines that inhibit insulin secretion) [10, 11].
Parasympathetic nerves are responsible for the early phase of insulin secretion, including the cephalic phase (i.e. insulin secretion, which occurs during anticipation of eating). In general, parasympathetic stimulation is believed to increase the release of insulin, glucagon, somatostatin and pancreatic polypeptide in many different species (for review, see [10, 11, 14, 15]).
Sensory nerves are also involved in the regulation of hormone secretion by endocrine cells [11]. Following chemical destruction of sensory nerves (capsaicin treatment) in mice, there is an increase in insulin secretion in response to glucose compared to control [81].
In conclusion, it should be added that pancreatic innervation is insufficiently studied, especially in humans [40, 44]. Interestingly, the innervation of the islets is very plastic: it has been shown that islets transplanted into the portal vein of diabetic rats were reinnervated by the nerves of the liver [82]. This makes it necessary to further study the role of innervation in the regulation of glucose homeostasis and plasticity of the endocrine part of the pancreas.
Despite the clinical importance, data concerning pancreatic innervation during human ontogeny and in diseases are very limited [37]. Such studies have been performed on rodents and mostly concern the sympathetic innervation [43, 55, 83]. The embryonic sources of neural elements are fibres of the vagus (n. vagus) and splanchnic nerves (n. splanchnicus) growing into the developing pancreas and neurons that differentiate from the neural crest cells migrating to the pancreas. Sympathetic fibres innervate the developing mouse pancreas starting from the 15th day of embryonic development (E14.5) [43]. Consequently, the degree of sympathetic innervation increases until 20 days of postnatal development (P20) [55]. The development of the pancreatic sympathetic innervation depends on nerve growth factor (NGF) [43].
The human pancreas receives extensive innervation, showing peculiar growth dynamics during gestation [37]. Ingrowths of nerves in the human pancreas start at 6 weeks of development. Further morphogenesis of pancreatic innervation is characterised by the increase of sources of innervation and degree of nervous element differentiation [84, 85]. Large bundles of nerve fibres and groups of poorly differentiated neurons are found in the human pancreas starting from the 8th week of development. At the end of the 9th week, the pancreas is innervated from almost all sources, characteristic of adults (celiac plexus, superior mesenteric plexus and posterior vagal trunk) [85]. In 1940, it was shown that pancreatic nerve cells migrate from the solar plexus and from ganglia located in the wall of the duodenum and along the branches of the vagus nerve (mainly right). At the same time, neuroblasts were detected in the pancreas of 20-week-old foetuses. Moreover, even in newborns pancreatic nerve cells were neuroblastic [86].
The gradual branching of the vascular and neural networks is observed in the human pancreatic development. Primitive free nerve endings are detected starting from the 12th week of development. In an immunohistochemical study of pancreatic innervation development in human foetuses, two peaks of increase in the number of structures of the nervous system in the head of the gland were revealed at the 14th and 22th weeks. In the pancreatic body and tail, the number of nerve structures increases from the 20th week [37]. By 30–32 weeks of development, the density of nerve endings is reduced compared to previous periods [85]. The innervation of pancreatic islets in humans is formed from the 14 to 15th weeks of the development. It differs from experimental mammals (rodents): the development of pancreatic islet innervation in rodents (mouse, Mongolian gerbil and golden hamster) is observed in the first weeks after birth [83, 87, 88].
Our study was performed on a collection of pancreatic autopsies, which allows us to explore the features of intrapancreatic innervation directly in humans using a variety of methods: classical histology; immunohistochemistry; light, fluorescent and confocal microscopy; morpho- and stereometry; statistical analysis; 3D histology; and computer reconstruction. The study was performed on 50 pancreatic autopsies of foetuses from the 10th to 40th gestational week (g.w.). Foetal pancreatic autopsies were divided into four groups according to the classification of the foetal period: pre-foetal period (10–12 g.w.), early foetal period (13–20 g.w.), middle foetal period (21–28 g.w.) and late foetal period (29–40 g.w.). A panel of antibodies for nervous system proteins (chromogranin A, neuron-specific enolase (NSE), neural cell adhesion molecule (NCAM), synaptosomal-associated protein of 25 kDa (SNAP-25, peripherin, S100 protein and neuron-specific class III β-tubulin), endocrine cell hormones (insulin, glucagon and somatostatin) and epithelial cells (cytokeratin 19 (CK19)) were used in this work [89, 90]. We generated new data concerning the spatio-temporal distribution of the innervation in the human pancreas during prenatal development.
In the pre-foetal period (10–12 g.w.), large weakly branched bundles of nerve fibres and nerve ganglia were detected already at the 10th week of gestational development using antibodies to NSE, NCAM and neuron-specific β-III tubulin (Table 1). The largest bundles of nerve fibres were detected in the dense peri-pancreatic mesenchyme, and the group of neurons and bundles of nerve fibres of smaller diameter were located in the loose mesenchyme between pancreatic ducts (Figure 1a). A network of fine nerve fibres was not developed. In some cases, bundles of nerve fibres were found near large vessels. Nerve ganglia in the pancreas of 10–12 week foetuses were small groups of cells.
Markers | NSE | NCAM | Neuron-specific β-III tubulin | S100 protein | Chromogranin A | SNAP-25 | Peripherin |
---|---|---|---|---|---|---|---|
Nerve fibres and ganglions | 10 weeks | 10 weeks | 10 weeks | 12 weeks | 14 weeks (weak staining) | 14 weeks | 14 weeks |
Endocrine cells | 12 weeks | 14 weeks | 14 weeks | 15–16 weeks (some islets cells) | 12 weeks | 16 weeks | — |
Appearance of immunopositive reactions to neural proteins in the developing human pancreas.
Spatio-temporal distribution of the nervous system structures in the human pancreas during ontogenesis. (a, b, d–f) double immunohistochemistry on the pancreatic slices of foetuses ((a) 12 g.w., (b) 16 g.w., (d) 28 g.w.), child ((e) 3 months) and adult ((f) 88 years): (a, b) insulin (blue) + S100 (red), (d, e) insulin (red)+ NSE (blue) and (f) glucagon (red) + NSE (blue). Arrows indicate some ganglia. (c) Stack of serial immunofluorescence images of NIC in the foetal pancreas (20 g.w.) (sum thickness of slices 90 mkm): Glucagon (green) + S100 (red).
Starting from 12 weeks, cells immunopositive for antibodies to S100 protein were found in nervous system structures. Localisation of neuromarkers was different. In the nerves, NSE-positive fibres formed the core, while small S100-positive cells surrounded them. The ganglionic cells were NSE-positive, and the small cells surrounding them S100-positive. The bodies of ganglion neurons were immunonegative to S100, that is, the positive reaction to S100 protein was observed in satellite cells of intrapancreatic ganglia and in Schwann cells of nerve fibre bundles, while NSE was detected in neuronal bodies and processes. In addition, NSE- and chromogranin A-positive endocrine cells were first found in 12-week foetuses (Table 1).
The formation of the human pancreatic islets starts only at 12 weeks of development. In the pre-foetal period, only contacts between single endocrine cells or small groups and fine nerve fibres were detected, and classical NIC I and NIC II were not found. At gestational week 10 (postconception week 8), thickening of the ductal epithelial layer was found, in which endocrine cells were concentrated forming “buds” on pancreatic ducts. As development proceeds, buds containing different types of endocrine cells separate from the ducts forming small clusters or mantle-type islets. In our studies, contacts between the structures of the nervous system and epithelial cells of primitive ducts were detected in the foetal pancreas at early stages of development (10–13 weeks) before the formation of islets.
The formation of the pancreatic lobules begins in the early foetal period, from 13 weeks. At the same time, active formation of the islets of Langerhans and innervation of the endocrine part starts (Figure 1b). Nervous system of the pancreas of 14–15 week foetuses becomes more branched in comparison with 10–12 weeks of development. Large bundles of nerve fibres are localised in the connective tissue of gland’s capsule. Smaller nerves pass into the interlobular connective tissue separately or along the blood vessels. Nerve fibres and ganglia are first found within the lobules. At the 16th week of development, the nervous apparatus of the pancreas is presented by bundles of nerve fibres of different diameters and nerve ganglia, which are located in the interlobular connective tissue and within the lobules. The nerve fibres connecting two nerve ganglia were found in 14–15 week foetuses, i.e. the first clearly detected integration of the nervous system structures was shown.
Localisation of antigens in the structures of the nervous system was also similar with the pre-foetal period. In addition, the immunopositive cells for chromogranin A, SNAP-25 and peripherin were detected in the nerve fibres and ganglia starting from 14 to 15 weeks of the development (Table 1). SNAP-25, NCAM, NSE, peripherin and neuron-specific β-III tubulin were detected in bundles of nerve fibres of different diameters and the bodies of neurons in human foetuses. However, there were fine nerve fibres located in the acinar parenchyma that were immunonegative for peripherin but reacted with other markers in all investigated cases. This suggests that nerve fibres of the human pancreas differ according to the set of expressed proteins. In addition, positive immunostaining for NCAM and neuron-specific β-III tubulin was observed in endocrine cells starting from 14 weeks of development, while SNAP-25-positive endocrine cells were detected only from 16 weeks of development. Immunopositivity to antibodies against S100 protein was found only in some islet cells starting from 15 to 16 weeks of development (Table 1).
The contacts of nerves fibres with endocrine cells were detected starting from 12 weeks of development. Already in the early foetal period, it was possible to identify NIC I (single insulin- or glucagon-containing cells in ganglia (Supplementary Video 1) or ganglia associated with the islets) and NIC II (single endocrine cells in the nerve (Supplementary Video 2), nerve endings associated with single endocrine cells or with the islets) and make their 3D reconstruction. The analysis of three-dimensional reconstructions allowed us to show ganglia associated with two islets at once, islets associated simultaneously with two ganglia, and NIC of mixed (intermediate) type [91]. Moreover, in the foetal pancreas, starting from 13 weeks, we showed simultaneously neuro-insular complexes and contacts between the structures of nervous system and epithelial cells located in ducts as well as in cell clusters that were often connected with the ducts. Based on these findings, we suggested that the development of neuro-insular complexes may be due to integration between the structures of the nervous system and epithelial progenitors at the initial stages of islet formation. Furthermore, endocrine cells are supposed to migrate along nerve fibres from the ducts, small clusters of endocrine cells and islets to the other islets, which are located a distance from pancreatic ducts, due to exocrine pancreatic growth, thus increasing their pool of endocrine cells. We suppose that the mechanism of pancreatic islet formation is similar to the formation of some peripheral analysers.
The pattern of immunoreactivity of neural markers during the middle (21–28 g.w.) and late foetal periods is similar to those in the early foetal period. In the middle of the foetal period, the density of pancreatic innervation is higher than in the early foetal period (Figure 1c, d). Despite increasing the size of pancreatic lobules and more sparse distribution of large and medium bundles of nerve fibres, the network of fine nerve fibres gradually branch and become denser. However, during late foetal and neonatal development, this network is much sparser (Figure 1e). This is due to the increase in the size of lobules. However, at all stages of human prenatal development, density of distribution of the nervous system structures is higher than in adults (Figure 1f). The density of NIC distribution also gradually decreases at birth. Our quantitative data indicate that the largest number of NIC I was observed in the early and middle foetal periods, during the active morphogenesis of pancreatic islets, whereas at birth (in the late foetal period) and in the adult, NIC II became more prevalent [91]. During the middle and late foetal periods, the nervous system components also contact epithelial cells located in ducts or in clusters outside the ductal epithelium and form complexes with separate epithelial cells. We observed CK19-positive cells inside the ganglia and nerve bundles, which were located separately or integrated within the islets [90].
In this study, our previous data were confirmed and refined [89] that the formation of the nervous system in the development of human pancreas can be divided into three stages. In the pre-foetal period, the nervous apparatus of the pancreas is represented by slightly branched bundles of nerve fibres and nerve ganglia. However, the structures of the nervous system differ from the late foetuses and adults by antigenic composition. Expression of various neural proteins does not begin simultaneously in the foetal pancreas.
The second stage of development of the nervous apparatus of the pancreas (during the early and middle foetal periods) is characterised by gradual branching of the neural network and formation of connections between the structures of the nervous system and exocrine and endocrine parts. In the early foetal period, nerve fibres gradually branch, nerve fibres and nerve ganglia appear localised between the acini, and a network of fine nerve fibres starts to form. In the later stages of development, the distribution of neural structures (nerve fibres, nerve ganglia and parenchymal network of fine nerve fibres) become sparser with increase in the size of the pancreas. Thus, innervation of the pancreas at this stage of development gradually becomes similar to the distribution structures of the nervous system in the adult pancreas.
In our studies, we demonstrated close integration between the structures of the nervous system and endocrine cells in the human pancreas, which were more frequently observed during prenatal development. Thus, a dense network is formed in the developing human pancreas, in which the structures of the nervous system are associated with the islets of Langerhans. The close relationship between developing islets and structures of the nervous system suggests that neuroendocrine interactions can influence not only the secretion of hormones but also to participate in the morphogenesis of the islets, presumably due to the participation in migration of endocrine cells from ducts to islets. Understanding the role of NICs in islet formation can lead to new approaches to understanding the mechanisms and treatment of diabetes.
Thus, our knowledge about the peripheral nervous system in the human pancreas is limited. Importantly, human islet development has not been examined for the presence of classical markers of the parasympathetic and sympathetic nervous systems. Furthermore, the exact location where neuronal axons terminate within the human islets in adults was not shown until recently.
However, the human pancreas is abundantly innervated during the gestational period. The value of such an abundant innervation of the pancreas and pancreatic islets, in particular, in human development is not clear. The observed differences between the nervous apparatus of foetuses and adults may have functional significance for pancreatic morphogenesis. Interestingly, some authors have described similar dynamics of innervation development in other internal human organs. The close relationship between the nervous and endocrine systems makes it necessary to further study the role of innervation in the plasticity of the endocrine pancreas both during formation of endocrine function and disorders of carbohydrate metabolism.
This work was supported by the Russian Foundation for Basic Research, project no. 18-015-00146.
The authors declare no competing interests.
The 21st century is, according to Dede [1], quite different from the 20th in regard to the skills people need for work, citizenship, and self-actualisation. Proficiency in the 21st century differs primarily due to the emergence of sophisticated information and communication technologies (ICTs). All over the world, ICT in education has been incorporated into formal national guidelines of the degree requirements of teacher education as an official policy. Digital technology in itself is often seen as a catalyst for educational change, and technology as a symbol for change is often understood as something positive, as investments in technology supports development in society [2].
\nDespite the fact that a fifth of the 21st century is behind us, it seems we are not up to speed regarding the skills anticipated as central for our digital era. Furthermore, there is a lack of clarity regarding what 21st century skills really are. The digital revolution is part of the change making 21st century skills different from those learned in schooling through the 20th century. ICT is changing the nature of perennial skills that are valuable in the modern world, as well as creating new contextual skills necessary for digital societies [1]. The world has changed fundamentally in the last few decades, and in effect, the role of learning and education has changed. Many of the skills needed in past centuries, such as critical thinking and problem solving, are, according to Trilling and Fadel [3], even more relevant today. How these skills are learned and practiced in everyday life in the 21st century though, is rapidly shifting.
\nThis chapter presents a critical perspective on how learners’ information, media and technology skills can be understood, and how they are connected to learning and innovation skills. Data for this chapter is based on qualitative in-depth interviews of ten teaching educators at the University of Waikato in New Zealand and ten teaching educators from UiT, the Arctic University of Norway. Both countries are facing similar educational challenges when teaching in digital environments, as both must educate teaching students in digital-rich environments with high access to various ICTs and educational resources at home [4]. The universities are similar in size and student numbers.
\nThis comparative study of Norwegian and New Zealand teaching education has led us to question how we educate students to meet the future and whether the educational systems are adapting sufficiently to new digital learning contexts. Is teaching students’ deep learning and critical thinking at risk of being limited in digital learning environments? In short, are students sufficiently prepared for the future?
\nThere is widespread agreement among educators and the public about the importance of the traditional fundamental building blocks that underpin student learning. These skills are often referred to as the 3Rs—reading, writing and arithmetic [5]. These are important skills, but as Crockett et al. [6] have argued, for students to progress from the foundations of learning, teachers need to expand their thinking outside their ‘primary focus and fixation on the Three Rs (3Rs)—beyond traditional literacy to an additional set of 21st century fluencies, skills that reflect the times we live in’.
\nThe notion that the 3Rs are not sufficient when preparing students for the future is not a new idea. Broader skills are needed and have been discussed since the first half of the 20th century. One example is an informal meeting of college examiners attending the 1948 American Psychological Association Convention in Boston, which was the start of the development of the theoretical framework known as Bloom’s taxonomy. This is a well-known and commonly used system of classifying the goals of the educational process beyond the 3Rs [7]. A common ground in the search for 21st century skills is by Keane, Keane and Blicbau [8] described as the 4Cs:
Critical thinking
Communication
Collaboration
Creativity
This understanding is based on three influential organisations associated with education, management, and industry developed definitions for 21st century learning. These organisations are the Ministerial Council for Education, Employment, Training and Youth Affairs (MCEETYA), the American Management Association (AMA), and AT21CS, a public and private partnership among governments, educators, academics, and industries [8]. While basic skills such as numeracy and literacy remain essential building blocks for learning, higher order skills such as the 4Cs are equally vital for learning and employment in the 21st century. Keane and Blicbau [5] write that 21st century skills are about fusing the 3Rs and the 4Cs, but the contextual aspect is also of great importance because context contributes to defining and affecting how different skills are used.
\nStudents in the 21st century live in a technology- and media-rich environment with access to a wide range of information, powerful digital tools, and the ability to collaborate and communicate with others. This affects what form of critical thinking is required. Fundamental to the development of 21st century skills is the importance of ICT for learning [8]. A discussion paper prepared for the European Union stated that information and communication technology (ICT) is at the core of 21st century skills. It is regarded as both an argument for the need for these skills, and a tool that can support the acquisition and assessment of them. The rapid development of ICT also requires a whole new set of competences related to ICT and technological literacy [9].
\nKeane, Keane, and Blicbau [8] write that using these technologies in education matter because students need to be prepared this digital world, in which they require a skillset that is broader than the traditional foundations of the 3Rs. Tucker and Courts [10] claim that teachers who mainly concentrate on a fixed curriculum that focuses on learning through repetition and memorisation find it difficult to connect new technologies to the traditional view of classroom learning.
\nTo be effective, teachers and students need to be able to demonstrate both the 3Rs and the 4Cs in relation to an online world. Government policy has been somewhat based on the assumption that access to technology is the key to achieving success. However, simply providing students with digital technology will not lead to development of these skills. How the teacher utilises these devices in the classroom is important for improved student outcomes [5]. Dede [1] claims that we need to move from consensus about the vision of 21st century learning to a thorough understanding of and commitment to the outcomes of 21st century learning. In reality, he claims, the ability to use digital devices in no way means that students know anything about global awareness or health literacy, learning and innovation skills, life and career skills, or even media literacy skills.
\nThere are new skills to master, and they must be understood intertwined with changing contextual skills. Trilling and Fadel [3] have an extended model, where the 4Cs are part of a skillset called learning and innovation skills. They propose two extended sets of skills: information, media and technology skills; and career and life skills (see Table 1).
\n1. Learning and innovation skills | \n2. Information, media, and technology skills | \n3. Career and life skills | \n
---|---|---|
\n
| \n\n
| \n\n
| \n
Three components of 21st century skills [3].
It is important to keep in mind that digital technology in itself is just a tool. Keane and Blicblau [5] state that without an understanding of learning theory, the use of transformative technology may actually be ineffectual. So, to have digital competence for learning, technological skills must be understood intertwined with other sets of skills and knowledge, like learning and innovation skills (the 4Cs).
\nThis has been an ongoing discussion for centuries, and yet it seems like educational practices and systems are having trouble adapting to the espoused learning theories, required formal policy, and understanding of the need for these skills [11]. Keane and Blicbau [5] criticise education for using technology in schools at the enhancement rather than the transformative stage, meaning that tasks could be completed satisfactorily without using technology, and without really changing the task. They claim we need to better provide the appropriate situations that will allow students to develop skills using the 4Cs. Lund [12] claims that schools either lack a view of technology or operate with a view of technology that is at best reductionist. A central control and management mechanism in schools is a standardised test. These tests provide some insight into students’ learning outcomes, but if used unilaterally, may also risk the development of a limited dynamic practice. As Resnick [13] writes, when preparing children for the future, how learning outcomes are assessed must be reconsidered. We need to focus on what is most important for children to learn, not what is easiest to measure and evaluate. The same concern is expressed when discussing digital technology and education. If we are only concerned with measuring the effects of the use of technology, instead of examining how digital technology changes the school culture, we risk cultivating a reductionist approach and ignoring possibilities for innovation [12]. These challenges are not exclusively related to digital practices, as school traditions for learning have in general been criticised for being pacifying. Jordet [14] writes that Norwegian schools are characterised by sedentary activities where the students are placed in the role of passive recipients of handed down knowledge. Such educational practices give students few opportunities to unfold their relational, meaning-seeking, creative, exploratory, and intentional natures. He states that for schools to be able to contribute to children mastering their lives and becoming participants in work and society, the schools’ traditions, thinking, and practices must be changed to better support students’ self-realising and active natures. Oostveen, Oshawa, and Goodman [15] found that meaningful learning is far more likely if new technologies are recognised as providing transformative opportunities.
\nElstad [16] claims that young people born after 1980 have digital capabilities and are therefore regarded as digital natives, in contrast to older teachers who are described as digital immigrants when born earlier than 1980 [17]. Digital immigrants are in governing positions in education, both as policymakers and educators. Could important stakeholders’ lack of digital technology be the reason education is not keeping up to date with new learning theories? Most teaching students referenced in this study were born in 1980 or later and are considered digital natives. Prensky describes digital natives as ‘native speakers of technology, fluent in the digital language of computers, video games, and the internet’ [18]. In this chapter, we present teaching educators’ evaluations of their students and their learning processes. In other words, so-called digital immigrants are evaluating digital natives, but it is not merely their technological skills being evaluated. As mentioned, these skills must be understood as intertwined. Students’ learning and innovation skills, like critical thinking, are intertwined with their information, media, and technology skills, and both sets of skills must be trained. Combined, it creates the need for new contextual skills. Keane, Keane, and Blicblau [8] write that simply using technology does not guarantee that deep learning will occur. The use of technology needs to align and adapt with our knowledge of learning to be able to operate in a transformative space.
\nA study of teaching students and their educators showed that teaching educators scored higher on professional digital competence than their students, but were more critical towards the technology in educational contexts than their students [2]. The differences between teaching educators and teaching students in this study were mostly unrelated to being digital immigrants or natives. They were connected to the complex competence gained through professional practice, regarding the interaction of content knowledge, pedagogical knowledge, and technological knowledge [19].
\nKnowledge of technology is only one critical component of teachers’ use of technology in their practice; they also need to know how to use it for successful integration in teaching and student learning. Being critical is not necessarily about being behind and not up to date, but about taking steps aside to gain a deeper perspective. Successful teaching is not only about finding the right technology, but also the values, norms, and attitudes that reside within the academic staff in teacher training organisations [2].
\nOne group of digital natives is defined as Generation Z. Tucker and Courts describe Generation Z as those who were born after 1990 [10]. This generation is described as ‘technically savvy, well adapted at communicating via the internet, and used to instant action due to the internet technology they have always known’. The traditional education model has, according to Tucker and Courts [10], been slow to adapt to the learning styles of these students, and researchers across the globe seem to agree on this. What seems more unclear is an understanding of what form of adaptation is needed, and how we get there. How do Generation Z’s learning styles and strategies affect learning processes in education?
\nDeep learning involves paying attention to underlying meaning. It is associated with the use of analytic skills, cross-referencing, imaginative reconstruction, and independent thinking. In contrast, surface learning strategies typically place more emphasis on rote learning and simple descriptions [20]. Deep approaches differ from surface approaches, where reproducing knowledge and syllabus-bounded practices is central. A third approach is the strategic approach, which is based on a competitive form of motivation and attempts to maximise academic achievement with minimum effort [21]. One tool for understanding deep learning is Biggs and Collis’ [22] developed structure of observed learning outcomes (SOLO), which form the basis of the SOLO taxonomy. The SOLO taxonomy focuses on the development of surface understanding to deep understanding, with a continuum of complexity and response to learning across the hierarchy of its levels of understanding. The SOLO taxonomy illustrates different levels of understanding:
Prestructural understanding is described as incompetence.
Unistructural understanding where relevant aspects can be identified.
Multistructural understanding where aspects are combined and described.
Relational understanding integrated in multistructural understandings. Being able to analyse, apply, argue, and compare aspects of one’s understanding.
Extended abstract is when the learner is able to create, formulate, generate, hypothesise, reflect, and theorise based on a relational understanding.
The higher the levels of understanding in the SOLO taxonomy, the higher the level of critical thinking, creativity, and communication. Critical thinking is the discipline of actively and skilfully conceptualising, applying, analysing, synthesising, and/or evaluating information gathered from, or generated by observation, experience, reflection, reasoning, or communication [5, 8]. All these aspects are central for 21st century skills and deep learning.
\nWhen teaching educators are asked about students’ learning processes, there is great concern regarding their ability to apply deep learning approaches. This is a complex field with a range of perceptions and understandings. Many of the teaching educators expressed conflicting views, where they addressed challenges and described how digital technology was fostering learning. In this chapter, we focus on the challenges of teaching with digital technology, and not so much on the benefits, which are many.
\nThis study is based on an explanatory sequential design, in which a conducted survey comprises the first phase of a sequence of methods. It is a comparative study involving 64 Norwegian participants from UiT, the Arctic University of Troms, and 44 New Zealand participants from the University of Waikato, with a response rate of 83.8% and 73.4%, respectively. The survey builds on Argyris and Schön’s theory of action [23] and consists of three main constructs: professional digital competence, professional attitudes towards digital technology in education, and professional application of digital tools.
\nBased on their results, ten participants from each university were invited to participate in an in-depth qualitative interview.
\nThe first step in strategically selecting interview participants was to ensure that all participants had high digital competence, with the aim of gathering informed opinions regarding the use of technology in educational contexts. The second step was to select participants within this group of digitally skilled teaching educators based on maximum variation sampling. Maximum variation sampling is a purposeful selection of participants with different perspectives on a phenomenon [24]. As Creswell [24] explains, the maximum variation sampling strategy requires defining a category that produces different responses to paint a varied picture of the participants. The category attitudes towards digital technology was used to select five participants who responded more critically and five participants who responded more positively towards digital technology within each country (Figures 1 and 2).
\nSelection of Norwegian teaching educators.
Selection of New Zealand teaching educators.
A total of 20 semi-structured interviews were conducted to understand and elaborate upon the results of the survey. The transcribed interviews were subsequently analysed using NVivo. One must consider the uncertainty arising when translating from one language to another. The survey, interview guide, and participant statements were translated from Norwegian to English. There are nuances when translating and analysing that may be lost, and these could have influenced the results. An ongoing collaboration with New Zealand researchers throughout the process was very helpful in concept- and language-related clarifications.
\nThis builds on a comparative study, but findings showed that the challenges experienced were evident in both countries. Despite being from different sides of the globe, teaching educators from both Norway and New Zealand expressed a concern regarding students’ learning in digital contexts. Overall, 13 of the 20 interviewed teaching educators expressed a concern regarding students’ deep learning, critical thinking, and source criticism. They link the students’ lack of learning and innovation skills with their level of digital literacy skills (cf. Trilling and Fadels’ model of 21st century skills). If their learning and innovation skills are not high enough, their use of digital technology seems to be at risk of not being used at a transformative level, and in some instances limits the quality of their learning processes.
\nOne of the teaching educators was quite astonished that students could be very technically competent without being able to search the web for knowledge. He explained that he had bachelor students not able to find literature, and when he demonstrated, the students were blown away as if it was magic. The ability to make use of keywords when searching for information and relevant articles was poor among students, he said, and he was surprised by the fact that they were not able to use the knowledge they ought to have attained during their education.
\nAnother teaching educator claimed that the students’ learning approaches were superficial and based on surface learning. She explained the reason was that they had not learned or practiced deep learning processes. ‘When asked to read a text, they do not extract what is important and relevant. They just dutifully read to complete the task’. She said it was fine that they were using Google when studying, but the worry was that the content seemed to move straight from the screen and out of their mouths, bypassing the students’ own relevant reflections. Another teaching educator claimed that there was an evident difference between students who had studied media and communication at the senior level in school and those who had not. They understood that there was quite a lot of work involved in being able to utilise the digital tools in a productive way, while the rest was basing their learning processes on a copy-paste strategy. She explained that students tended to express a strategy of searching for readymade abstracts online. This was very unfortunate because the type of learning we want to promote in our teacher education is largely based on reflection, not just reproduction of readymade connections between levels of understanding.
\nI asked the teaching educators if it was a challenge to get students to engage in deep learning when readymade answers were easily assessable online. The teaching educator replied, ‘Of course’. He explained how he had noticed that students were often using online references instead of the syllabus. ‘It can be the same keywords as is described in our syllabus, but they would rather google it. So, that is when I question what source criticism they have applied to secure their information’. He explained that the students were not concerned with this, and uncritically used this on tests and exams. One critical question to be asked was: When using a traditional lens when assessing the students, what are we measuring as new tools and contexts for learning have transformed learning activities and outcomes? Do we have practices for evaluation that aligns with the new learning activities and intended outcome?
\nThe same teaching educator’s experience with digital tools was that they were not always helpful. Furthermore, he felt it somewhat distorted/disabled the learning processes. This understanding was confirmed by another educator who explained that she thought of digital technology as a detour. ‘Sometimes we use digital technology like PowerPoint, when traditional methods like using a black board can work as a better tool’. She explained that students expressed their preference for educators using PowerPoint, as they found it better not having to write everything down.
\nIn New Zealand, teaching educators were also vocal regarding this challenge. One teaching educator explained how she had noticed that students were increasingly entering search words in Google to access what she referred to as ‘easy takeaway knowledge’. The consequence, she explained, was that the students did not have to engage deeply or really work with the content. ‘Students can access it very easily, and it almost replaces thorough research, like reading academic articles,’ she said. She explained how this availability of a lot of information on the internet undermined students’ capacity to read critically, do research, and read academic journals or chapters. She elaborated that this aspect of availability, quick easy access, was undermining the development of academic capacities and serious research for assignments. A critical selection of information takes more time. ‘You have to actually digest those harder articles, and it seems to me that students read less of those […] even if they use them in their assignment it is superficial.’ Another one supported this perception and explained: ‘the easiness of technology creates a false notion of what learning is about, that you don’t have to work for knowledge. I don’t think that’s true. If you look at anyone who is good at something, they have put in a lot of work and practice. I think digital technologies might be kind of responsible for this notion of learning’.
\nSome research shows that students who often use technology tend to do worse when compared with students who use less of such tools [4, 25, 26, 27]. Mueller and Oppenheimer [28] conducted a study in which they concluded that the use of a laptop negatively affected the students’ test results. They focused on the students’ use of laptops instead of traditional writing during lectures. They argued that note taking by hand calls for different cognitive processes than writing on a laptop. One can write faster on a laptop and take more notes. ‘Although more notes are beneficial, at least to a point, if the notes are taken indiscriminately or by mindlessly transcribing content, as is more likely the case on a laptop than when notes are taken longhand, the benefit disappears’ [28]. Writing by hand is slower, and one cannot take verbatim notes in the same way as with a laptop. Instead, students listen, digest, and summarise so that they can succinctly capture the essence of the information. Taking notes by hand forces the brain to engage in deeper learning, which fosters comprehension and retention [29, 30, 31]. As May points out, ‘even when technology allows us to do more in less time, it does not always foster learning’. This is in line with the teaching educator who claimed that that learning has a tendency to be too easy. When students are copying and pasting from the internet and using digital technology uncritically, they miss out on the constituting process of struggling with individual concepts and developing their 21st century skills, like reflecting, generating, being creative, theorising different concepts, and communicating independent ideas. It seemed like the teaching educators had trouble engaging students in deep learning processes as digital technology created a learning environment that fostered the strategic approach, and they experienced challenges where students attempted to maximise academic achievement with minimum effort. Perhaps they did this unaware of the consequences these approaches could have on their potential learning outcomes.
\nDeep learning strategies cannot be externally imposed and must be interest-led. Interest can be stimulated by placing less emphasis on curriculum content and more on contextual interpretation, in other words, the 4Cs [20]. Learning activities need to be interesting and engaging and allow critical reflection and dialogue with peers and mentors [32].
\nCritical thinking is vital for problem solving, but one teaching educator explained that students’ critical thinking skills were virtually non-existent, and that a lot of effort was put into trying to develop those skills alongside their digital skills. Another explained that as much as digital tools were creating opportunities in teaching, they were also creating challenges. Those challenges were related to teaching students to be critical. When is it useful to use it, and what resources are usable in academic settings?
\n‘The students’ ability to use and utilise digital tools shocks me, because it is very poor. They are consumers; they are not producers. The job we do here is about making them able to become producers as well, so that they can utilise the learning resources available. They need to be prepared better through high school in relation to the critical use of digital tools; there are many who have major shortcomings. I think it has gotten worse really, because it’s like if it’s not on Facebook or Google, then it does not exist. It’s a little scary. It seems that they are becoming less and less aware that it is just a person who has written this, and that information could have been written with underlying agendas. The critical reflections are something we have to work quite a lot with, and more for each new class just the three years I have been here.’ (translated from interview).
\nOne teaching educator related the challenge to the fact that it was very easy to retrieve information, without necessarily understanding what it means. One can just type in a word or look something up, ‘then you just read exactly what comes out, because you typed in a word’. The problem, she explained, was that the students were not able to see the whole picture. It was noticed in their presentation on exams, or in things they wrote, that they did not fully understand the concepts they were writing about. Their presentation was really just reformulation of something copied from the internet, and was not coherent.
\nOne challenge is related to what extent they understand the concepts they are writing about; another is whether the source is trustworthy. The students were warned both in writing and orally, one teaching educator explained, not to use bloggers’ opinions and secondary interpretations as a basis for academic writing. The students still handed in papers with hardly any syllabus literature or academic references. One teaching educator explained that she had been teaching for so long that she remembered well the time when education was much more book centred.
\n‘One had to search for and order different articles at the library, and so on. Now it is all online, and that is great. It makes things easier. From that perspective, the students have accepted the possibilities online, and that is good. Nevertheless, there is a negative side to this. I do not find that students’ source criticism has developed or increased according to this change. For instance, I do not accept references to Wikipedia in my papers, even if there is a lot sensible information written there. I encourage them to start there to get an overview. It can function as a platform for relevant references. But they have to be critical regarding what they are basing their arguments on, and the skills to do this are lacking.’
\nThe same perception is widespread among the New Zealand teaching educators. One explained that one of the things they were focusing on was critical analysis and information literacy. He said, ‘The information is at our fingertips, but we need to really think about when we’re using it and how it’s being used, and be able to seek out robust information for what we need, and understand exactly what we’re using’. Another participant explained that she had noticed that there was an overreliance on inaccurate media rather than knowing that they could go to a particular resource and have more valid information.
\n‘So they can’t make those kind of judgements about what is valid and what isn’t valid to cite, because there’s been no role models for them to look at and learn from. So the whole concept to any kind of academic approach to writing, whether it is through social media or other aspects of writing, is a very big learning curve for them… they struggle.’
\nThe same challenge was exemplified by an interaction with another teaching educator and a student.
\n‘One of my postgraduate students this week wanted to know what I meant by “doing critical review”, which is an instruction for an assignment. And she copied something in, and I said: Where did you get this from? She said: Oh, I got it off Mr. Google, and I’m sort of thinking is this really, you know… This is a postgraduate student who is saying that, and doing that. That is actually pretty problematic. So, you can’t make too many assumptions about where people are at.’
\nShe explained that the biggest challenge was that the students needed to develop their critical perspectives on what they were seeing, and referred to this as ‘very patchy’. She was trying to encourage academic writing, thinking, and discussion, to make students extract knowledge and the underpinning ideas. To ‘have the students in the position where they can tell the good from the bad, the useful from the not so useful information. That has been a problem.’
\nOne teaching educator challenged the notion of students as superficial in their learning because of digital technology; she claimed that the challenge was about the need for a different set of skills.
\n‘I certainly don’t feel that students are more superficial because they\'re using them, or because they can access Wikipedia or… I think they need to learn a different set of skills, but I think that once you have developed those skills, I think you can actually get into deeper learning, and I think digital technology enhances those skills. I think we can be superficial in whatever we do. But, it’s not because of digital technology we become superficial.’
\nBased on what the teaching educators explained, it seems like digital learning environments are enabling advanced multi-structural learning at such a high level that their lack of relational understanding and ability to create extended abstracts have been overlooked. Digital tools make students appear skilled in handling information as they can copy ready-made text online by googling keywords. This apparent skill in writing could be misleading for teachers in their assessment of the student. When students reach higher education, they are perceived as unskilled and uncritical, as higher education reveals a worrying lack of learning strategies that would enable them to reach deeper levels of understanding [22]. It seems that through primary and secondary education, they develop an imbalance between learning and innovation skills, and information, media, and technology skills [3]. Furthermore, this imbalance seems to create an asymmetrical reinforcing effect as digital environments make it easy to present multi-structural understanding at a high level, which can disguise the need to work with students’ ability to think critically, a central part of the higher order of thinking in the SOLO taxonomy.
\nThat ‘everything used to be better’ is a claim made by all generations. One teaching educator pointed out that ‘students in the past have also written things they do not understand themselves. I do not think that is new. Everyone just wants to find the easiest way to a good grade, maybe.’ However, if seeking the easiest way is a fundamental human trait, it is a challenge for teaching and learning now that knowledge is more easily accessible and presented, without engaging critical thinking and deeper cognitive processes. Wajcman [33] states that ‘Rather than simply saving time, technologies change the nature and meaning of tasks and work activities, as well as creating new material and cultural practices’. We need to adapt to these changing practices and learning activities, and adjust how we educate our students to be prepared in this new learning context. The teaching educators in this study had some suggestions.
\nTeaching educators in this study expressed a worry regarding the digital format versus traditional books. As information is more easily accessible, students tend not to read the books and research the greater context information it was gathered from. In a book, you often have to read larger sections to get a grasp of the concepts. When googling keywords, it is easy to find a lot of ‘hits,’ and then mix a selection of copied sections. This can apparently look like a reasonable text, but it is surface learning and without deep understanding of the content. Reading a book will perhaps create deeper learning, even though the text produced is less polished than a copy-paste text from already digested sections online.
\n‘I mean obviously, students have different skills, but I am thinking that critical thinking skills, reading hard information is definitely undermined, that is what I am thinking. I am noticing that with students.’ (New Zealand teaching educator)
\n‘I do not think their digital skills have become any higher in the last five years, I think almost on the contrary. They are very good at watching videos and looking for things online, but I do not think they are good at retrieving relevant information. They are not as source-critical as I would like. We probably have a job to do to make them able and skilled.’ (Norwegian teaching educator)
\nThe two skillsets, learning and innovation skills and digital skills, are connected. Students will not flourish in their digital skills if they are not intertwined with the 4Cs. Digital natives and Generation Z have a good technical understanding, but integrating that with the skills of being creative and critical is central to achieving deep learning processes in digital learning environments.
\n‘They (students) are not able to transfer those skills and understandings into their learning environment. I would say the key thing again here is that the students might come in with skills and abilities, but not necessarily pedagogical understanding of how to actually implement that in their teaching practice. I think that\'s the key thing that we, initial teacher education lecturers, need to really focus on, and I think we need to come up to the plate and think about the digital literacies our students have… and actually think about being responsive to those as well.’ (New Zealand teaching educator)
\nOne teaching educator who perceived students as getting shallower in their learning was vocal about the value of structuring education around the use of books as well as digital devices.
\n‘I require them to read a textbook, because I think that doing lectures actually, online, is actually not a satisfactory way to get one’s point across. So instead, what I do is I weave my points across all the ways that I teach each week, so all the things I present, all of my interactions and discussion groups and… I think it works up to a point, but I\'m expecting them to read the textbook quite well, really.’
\nTo round up this chapter, I leave the final word to one of the New Zealand teaching educators who summed up most of the main findings in our study.
\n‘I think digital technology can be a lot more passive at times, and in terms of students, I think they just see technology as providing the answer. I think it is important to challenge them and say, “There may not be an exact answer to the question; you have to keep challenging and questioning.” I sometimes believe they have become a lot more passive, and just accepting what comes via the technology as being the one and only, or the right way of doing things. Rather than challenging. I think it is due to the way the world has shifted. Where it is a lot easier for them to go online and get something, rather than physically having to go somewhere and think about it, like a library or hunt out a book, or… Everything is right there. Therefore, I think that passive learning most probably happens a lot more because of the technology, because they can just access wherever they are. In terms of preparation, coming through from high school, yes, I think there are some definite skills in terms of being critical of information that needs to be taught, prior to coming into higher education. Particularly in the sense of questioning the information they are accepting. I believe some disadvantages are that most probably the students do not challenge enough, they just accept technology, and I think that might be the way technology has been introduced over the years. “Here it is, here is the answer.” “If you don’t know, just google it, and you’ll get something.” So that passive, not questioning, not challenging… I think is a real disadvantage.’
\nIt seems that students’ development of critical thinking and deep learning is challenged in digital learning environments. A high level of ICT literacy seems to challenge the lens traditionally used to assess students’ capabilities and needs. Furthermore, ICT skills and learning and innovation skills seem to mutually influence each other, as low learning and innovation skills make the students’ ICT skills stagnate when assessing their critical use of online resources. We find that learning in a digital environment complicates the development of critical thinking, but we also believe that this can be corrected by redefining what it takes to prepare students for the future. For a long time, the focus has been on developing their digital skills. However, it would seem like we have not paid enough attention to what the digital transformation requires of interwoven aspects related to learning in digital societies. We need to develop the traditions in education, where the focus has been on technical skills more than on interdisciplinary competencies. If we are able to better secure and develop students’ abilities to be critical and creative, and to collaborate and communicate, digital learning environments could act as learning resources for all students. Without this skillset, there is a risk of students using digital resources in a way that prohibits deep learning and the development of higher order thinking. Based on the input of the teaching educators, it is essential that education is structured in a way that a lack of the 4Cs is noticed by educators and teachers, and that learning is structured to develop such skills. It is unfortunate if students acquire a high degree of information, media, and technology skills, as digital immigrants do, without the learning and innovation skills required to manoeuvre constructively in the overwhelming and easily accessible landscape of digital learning. Education needs to structure learning that challenges students to connect different skillsets, so new contextual skills and knowledge are developed. Just like critical thinking in digital spaces.
\nThe publication charges for this article have been funded by a grant from the publication fund of UiT The Arctic University of Norway.
\nWe pride ourselves on our belief that scientific progress is generated by collaboration, that the playing field for scientific research should be leveled globally, and that research conducted in a democratic environment, with the use of innovative technologies, should be made available to anyone.
\n\nWe look forward to hearing from individuals and organizations who are interested in new discoveries and sharing their research.
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