Middle East Journal of Applied Volume : 07 | Issue :04 |Oct.-Dec.| 2017 Sciences Pages: 857-869 ISSN 2077-4613

Neuroanatomical variability in the distribution of glycogen, collagen, Perineural glial cells among some Aves species inhabiting Egypt: Evidence for their role in cognitive behaviors

Hani S. Hafez1, Ahmed B. Darwish1 and Islam M.Hamza1

Zoology Department, Faculty of Science, Suez University, Suez, Egypt Received: 23 August 2017 / Accepted: 24 Oct. 2017 / Publication date: 23 Nov. 2017

ABSTRACT

Birds can execute cognitive primate-like behaviors, although their small-sized brains. This study investigated the glycogen and collagen distribution as well Perineural glial satellite cells among Hooded Crow (Corvus cornix), chicken (Gallus gallus domesticus), and pigeon (Columba livia domestica) brains. The highest neuron packing density levels were specific for hooded crows and distributed in the nidopallium and pallidum; Whereas, chickens dense neuron structures distributed in multiple brain areas such as mesopallium, nidopallium, and nidopallium caudalaterale; and pigeons have the lowest level of distribution in areas and density. The nidopallium caudalaterale of the hooded crow characterized by the presence of small area with small segmentation features. The distributed clustered glial cells (perineuronal satellite) of hooded crow were more than chickens and were absent in pigeons, which may be considered as one of the regulatory factors that boost higher cognitive abilities in hooded crows. Additionally, the glycogen and non-fibrillar collagen were more distributed over hooded crow brain regions than other species. These findings may assert that intelligence and cognition in birds depend on multiple factors or/and different areas that increase their synaptic plasticity and neural transmission. This study tried to explain and highlight the significant distributional role of the neuroanatomical glycogen and non-fibrillar collagen in different brain structures in regulating the cognitive behaviors in birds.

Key words: Hooded Crow, Chicken, Pigeon, Brain, Cognition.

Introduction

Bird brains are different to mammalian brains due to the non-shared anatomical structures before the divergence from the last common ancestor of 300 MYs. They are lacking the six-layered neocortex of mammals, but they share some feature similarities in the decision-making cells (Evans, 2000; Jarvis et al., 2005; Butler et al., 2011). Avian brains control their perceiving memory and conducting their sensory information abilities by special macrostructure and microstructure (Krushinsky et al., 1985; Zorina et al., 2006). The avian was divided into regions separated by fiber tracks (nuclear structure) and hyperpallium consists of stretched nuclei piled on top of one another through the dorsal–medial– anterior surface of the brain (Beckers et al., 2014). Jerison (1985) reported that bird brains may emulate many mammalian structures due to their large and complex anatomical structures and brain size/body weight ratio (Hunt, 2000; Pepperberg, 2002). Portmann (1947) suggested a ratio called Portmann’s forebrain/brainstem (FB/BS) index defined by the forebrain weight/ brainstem weight ratio of the Galliformes in comparison to their body weight. This study demonstrated that the minimal Portmann index values (3-4) were characteristic of the evolutionarily oldest species such as Galliformes and Columbiformes, whereas evolutionarily more recent species such as Parrots, Corvids, and owls had the maximal FB/BS index with 28, 18, and 17, respectively. So, he presumed that the FB/BS ratio index results may suggest that the avian evolutionary cumulative changes had an important role in their behavior On one side, Doyle and Watterson (1949) and DeGennaro (1959) assumed that significant extensive glycogen storage can provide a substrate for triggering metabolic pathways supporting central nervous system functions. On the other side, the non-fibrillar collagen type IV or basement

Corresponding Author: Hani S. Hafez, Zoology Department, Faculty of Science, Suez University, Suez, Egypt E-mail: [email protected] 857 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613 membrane collagen (Hudson et al., 2003) are particular structures found at tissue boundaries, underlying epithelial, endothelial, fat, muscle and nerve cells and increase in cell integrity. Collagen IV molecules are longer than the fibrillar collagens and containing several discontinuities in the (Gly- X-Y) repeat. Non-fibrillar collagens characterized by distributing C-terminal domain matricryptin which exhibits distinct function from their matrix molecule (Ramont et al., 2007). Matricryptins participate in axonal outgrowths, synaptogenesis, and synaptic plasticity in different species such as worms, flies, fish, and mice (Su et al., 2012; Wang et al., 2014). Furthermore, birds like crow show a high level of cognitive behavior and creativity with new- tool manufacturing due to their large anatomy of the and the pallium (Puelles et al., 2017; Weir et al., 2002; Hunt and Gray, 2003). The avian anatomical pallial structures possess two major subdivisions: the dorsal ventricular ridge (DVR) comprises the mesopallium and nidopallium and the Wulst containing the hyperpallium. Karten (1969) and Nauta and Karten (1970) stated that the structural neural connectivity among nidopallium and hyperpallium along with the thalamus, the visual-auditory plays a necessary role in the processing of the sensory inputs. Furthermore, the upper hyperpallium and the arcopallium produce descending projection neurons to diverse sensory and motor cell groups of the brain (the thalamus, midbrain, and hindbrain) and the spinal cord. The genoarchitectonic studies on the avian pallial structure during development revealed that the telencephalic subdivisions (the hyperpallium, the mesopallium, the nidopallium, and the arcopallium together with hippocampal complex and Piriform cortex) were derived from the developing telencephalic pallium from which , neocortex, claustrum, piriform cortex and pallial amygdala were derived in mammals (Smith-Fernandez et al., 1998; Medina and Reiner, 2000; Puelles et al., 2000). Cytoarchitectonically, the avian hyperpallium, nidopallium, and arcopallium are not striated like mammalian neocortex, but they carry out the same neural operations at the cellular level (Karten and Shimizu, 1989; Karten, 1991; Cohen et al., 1998; Jarvis et al., 2005). During phylogeny, the avian and mammalian pallium were originated from the dorsal telencephalon and was made out of four distinguished embryonic areas (medial dorsal lateral and ventral pallium). Both mammals and birds hippocampus have originated from the medial pallium. Mammalian prefrontal cortex developed from the adjacent dorsal pallium and is closely associated with the hippocampus; whereas, the avian nidopallium caudolateral (NCL) structure, similar to the prefrontal cortex, was developed from the ventral pallium and is farther off to the hippocampus (Mogensen and Divac 1982; Güntürkün 2005). The present study was conducted to explore the neuroanatomical variations of glycogen and collagen in pallial and cerebellum of three bird species (Corvus cornix), (Gallus gallus domesticus), and (Columba livia domestica) distributed in Fayoum governorate, Egypt.

Materials and Methods

Experimental animals:

The animal transportation and experimental procedures were done in compliance with the approval from the University of Suez Canal Animal Ethics Committee in accordance with the Animal Welfare Act. Six male hooded crows (Corvus cornix), six male chickens (Gallus gallus domesticus) and six male pigeons (Columba livia domestica), collected from the Fayoum region, Egypt were used in this study. Crows and pigeons were caught with traditional hunting nets and chickens were distinctive species in Fayoum caught from normal poultry sheds (no special permit required). Crows were differentiated as male or female by their morphological characteristics and body weight (Kenward et al., 2004).

Tissue preparation:

All birds were injected intramuscularly with a lethal dose of pentobarbital (30 mg/kg) (Ludders, 2008) and transcardially perfused with 0.9% saline followed by 4% paraformaldehyde solution. The brains were removed from the skull and immersed in 4% paraformaldehyde in 0.1 M sodium phosphate buffer followed by 30% sucrose in 0.01M phosphate buffered saline for 5 days. Brains cerebrum and cerebellum were sectioned coronally at 30 μm thicknesses using a cryostat and

858 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613 collected in phosphate buffered solution with 0.01% sodium azide. Sections were mounted onto gelatine chrome-alum coated slides.

Histology and histochemistry analysis:

Periodic acid–Schiff (PAS) technique:

Glycogen staining was carried out using Periodic acid–Schiff (PAS) according to the protocol of Thompson (1966). Briefly, selected brain sections were oxidized with 5% periodic acid for 10 min, stained with Schiff reagent for 30 min, dehydrated and mounted (Eukitt).

Mallory’s Trichrome stain for collagen:

Histological staining of collagen was carried out using Mallory’s Trichrome stain according to the protocol of Luna (1992). Briefly, mounted sections were rinsed in absolute alcohol for 1min followed by immersing in preheated Bouin’s fluid until became colorless. Dehydration carried out using absolute alcohol with 3 changes with 1 min for each and cleared with xylene.

Silver nitrate staining for nerve axon:

Staining of nerve cells and their processes was carried out using silver nitrate according to the modified protocol of Luna (1992). Briefly, mounted frozen sections dried for 5-10 minutes, rinsed in dH2O, and incubating in pre-warmed (40 ºC) silver nitrate solution for 15 minutes. One drop of concentrated ammonium hydroxide was added to the silver nitrate solution until the precipitate clearance. Slides incubated in the ammonium silver solution in a 40 ºC oven for 30 minutes or until sections became dark brown followed by rinsing in the developer working solution for 1 minute or less. Slides were washed 3 with dH2O and rinsed in 5% sodium thiosulfate solution for 5 minutes and followed by washing with dH2O and dehydrated with 95% ethanol. Sections were imaged using a Leica DM 2500 with a mounted Leica DFC 290HD digital camera and stacked using CorelDRAW X4. The cerebrum and cerebellum, brain areas were identified using the avian brain atlas according to the Avian Consortium Nomenclature (Reiner et al., 2004; Jarvis et al., 2005).

Results

The present study investigated the brain anatomy and histological differences of some bird species in Egypt, including Passeriformes, Corvidae (Corvus cornix); Galliformes, Phasianidae (Gallus gallus domesticus); and Columbiformes, Columbidae (Columba Livia domestic). Hooded crow (Corvus cornix) revealed the highest distribution rate of tightly-packed cell clusters identified as glial satellite cells among the other examined species. These clusters tightly packed in 3 to 5 cells and distributed in two forms, either enclosing neurons with a very short projection or no visible neuronal structure in hippocampus and parahippocampus, respectively (Fig. 1A). Moreover, periodic acid-Schiff (PAS) stain revealed a lot of separately distributed glial cells with dense glycogen, glycoprotein or glycolipids deposits. On one side, mesopallium and the thalamus showed high distributed clustered cell numbers (Fig. 1C, F); on the other hand, neither the hyperpallium nor the nidopallium and the pallidum contains clustered cells (Fig. 1B, D, E). Moreover, nidopallium characterized by different distributed motor neurons with triangular cell bodies and increased distributed protoplasmic astrocytes (Fig. 1D). The pallidum showed distributing nerve cell bodies with fine granules and pseudo-unipolar neurons in the cytoplasm (Fig. 1E). On one side, the tightly clustered perineuronal satellite glial cells detected among chickens (Gallus gallus domesticus) pallium area were in (hyperpallium and the nidopallium (Fig. 2B, D, respectively) and absent pigeons (Columba Livia domestica) (Fig. 3). On the other side, chickens and pigeons hippocampus revealed multiple rounded and triangular neuronal cell bodies with a variable number of projections (Fig. 2A; Fig3A).

859 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Fig. 1: Microphotographs in the cerebrum of Hooded Crow (Corvus cornix) stained with Periodic acid–Schiff (PAS). The clustered glial cells indicated by head arrows distributed in A) and B) The hippocampus; C) The mesopallium; D) The motor neuron cells in the nidopallium; E) Pseudounipolar neurons (Large hollow arrow) and individual glia (small solid arrow) in the pallidum F) Perineural galial stallite cells in thalamus.

Fig. 2: Microphotographs in the cerebrum of Chicken (Gallus gallus domesticus) stained with Periodic acid– Schiff PAS. A) Multiple neuronal cell bodies with variable number of projections and different shapes varied from rounded to triangular (normal solid arrow); B) The tightly clustered cells of perineuronal satellite glial cells indicated as arrowheads in the hyperpallium; C) Highly condensed, rounded nuclei with unstained cytoplasm in their cell bodies identified as oligodendrocytes in the mesopallium; D) The nidopallium.

860 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Fig. 3: Microphotographs of Pigeon (Columba livia domestica) cerebrum sections stained with Periodic acid– Schiff (PAS). A) Multiple neuronal cell bodies with variable number of projections and different shapes varied from round to triangular (normal solid arrow); B) Highly distributed cells with low to moderate cellular density and fried-egg-appearance with fusiform and rounded shapes in the hyperpallium; C) The mesopallium, D) The nidopallium; E) The . F) Normal distributed triangular neuron cells in Pallidum.

Fig. 4: Microphotographs of Hooded Crow (Corvus cornix) brain sections stained with Mallory's trichrome. A) The hyperpallium; B) Nidopallium; C) Pallidum and striatum; D) The thalamus.

861 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Fig. 5: Microphotograph of Chicken (Gallus gallus domesticus) brain sections stained with Mallory's trichrome. Shows the collagen distribution in hyperpallium, mesopallium, and Nidopallium.

On one hand, Gallus gallus domesticus mesopallium displayed highly condensed rounded nuclei with unstained cytoplasm in their cell bodies identified as oligodendrocytes (Fig. 2C). On the other hand, the pigeon's pallium and sub-pallium (the hyperpallium, the mesopallium, the striatum, and the pallidum) showed highly distributed cells with low to moderate cellular density. Furthermore, fried- egg-appearance cells with fusiform or rounded shapes distributed separately or conjugated as in the pallidum away from the neural cells (Fig. 3B, C, E, F). Finally, hooded crow (Corvus cornix) brains considered as the most species with high storage levels of glycogen bodies followed by chickens (Gallus gallus domesticus) and pigeons (Columba livia domestica) in order. Hooded crow (Corvus cornix) pallium showed the highest species with nonfibrillar collagen granules distributed in the nidopallium and the hyperpallium; whereas, its sub-pallium and thalamus characterized by a little distribution level and absent in the pallidum and the striatum (Fig. 4). In chickens, the highest level of distributed collagen granules was specific for the hyperpallium followed by the nidopallium and the mesopallium (Fig. 5). Pigeons (Columba livia domestica) collagen granules detected in the nidopallium (Fig. 6A), the nidopallium caudalaterale (Fig. 6B), and the pallidum, whereas the striatum distinguished by its low scattered collagen granules (Fig. 6A). The hooded crow and chicken cerebellum displayed high distributed non-fibrillar collagen and the granular layer was more than molecular layer (Fig. 8A, B, respectively); whereas, pigeons showed very low rates of collagen in both layers in pigeons. (Fig. 8C). In hooded crow, the silver nitrate stain indicated highly extended neuron fibers in the whole brain sections and showed the specific anatomical structure in nidopallium caudolaterale (NCL) with ~10 partition segments (Fig. 9A) together with highly distributed myelinated neurofilaments in the sub-pallial areas of the striatum and the pallidum (Fig. 9B, C). Moreover, highly condensed staining for collagen fibers distributed in the pallidum myelinated axon fibers (Fig. 9B) and Purkinje cells in the cerebellum characterized with short dendrites and single axon was found (Fig 9C). Chickens’ brain sections stained with silver nitrate revealed extended neurofilaments from the mesopallium to the nidopallium areas (Fig. 10A) with dense myelinated axons in nidopallium caudalaterale (NCL) forming an island-like shape (Fig. 10B). Furthermore, the pallidum and the striatum showed little to a medium distribution of myelinated axons, respectively (Fig. 10C, D). Pigeon nidopallium showed long myelinated axons with large pyramidal cell bodies and bi-branched- dendrites (Fig. 11A). The cerebellum characterized by small Purkinje cell bodies of long axons (Fig. 11B).

Fig. 6: Microphotographs of Pigeon (Columba livia domestica) brain sections stained with Mallory's trichrome. A) Shows nidopallium, the striatum, and the pallidum; B) the nidopallium caudalaterale.

862 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Fig. 7. Microphotographs of brain cerebellum sections stained with Periodic acid–Schiff (PAS). Blackhead arrow indicating the Purkinje cells and granular layer with highly concentrated glycogen content in A) Hooded crow (Corvus cornix); B) Chicken (Gallus gallus domesticus); C) Pigeon (Columba livia domestica) with less glycogen content.

Fig. 8: Microphotographs of brain cerebellum sections stained with Mallory's trichrome. A) Hooded crow (Corvus cornix); B) Chicken (Gallus gallus domesticus); C) Pigeon (Columba livia domestica).

Fig. 9: Microphotographs of Hooded Crow (Corvus cornix) brain sections stained by silver nitrate showed the myelinated sheath of nerve fibers. A) nidopallium caudalaterale partitions with multiple extended nerve fibers; B) extended nerve fibers and silver nitrate stained collagen in the pallidum; C) The striatum, D) Purkinje cells (arrowhead) and extended nerve fiber with dendrite (hollow arrow) in the cerebellum.

863 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Fig. 10: Microphotographs of Chicken (Gallus gallus domesticus) brain stained with silver nitrate. A) Extended neurofilaments from the mesopallium to the nidopallium, B) Island-like shaped dense myelinated axons in nidopallium caudalaterale (NCL), Medium distribution of myelinated axons in C) The pallidum and D) The striatum.

Fig. 11: Microphotographs of Pigeon (Columba livia domestica). A) long myelinated axons with large pyramidal cell bodies and bi-branched-dendrites in the nidopallium (arrowhead). B) small Purkinje cell bodies with long neurofilaments in the cerebellum (normal arrow).

Discussion

Brains are found in different shapes and sizes ranging from simple nerve nets to complex and layered structures found in vertebrate brains. Evolutionary processes triggered the development of new traits of different brain regions that have held and inherited to the descendants with simple nerve net serving the organism’s behavioral abilities (Roth and Dicke, 2005). Mammals and birds are more intelligent animals than others in the animal kingdom. Corvids, parrots, primates and cetaceans are the most intelligent birds and mammals, respectively. Social and ecological environments may be considered as one of the evolutionary processes triggering the intelligent behavior of animals through their innate responses or trial and error learning (Roth and Dicke, 2005). So, complex and uncertain environments could favor the costly strategy of intelligence (Godfrey-smith, 2001; Sterelny, 2003). Our results detected highly tight clustered glial cells distributed among hooded crows (Corvus cornix) and chickens varied in their number and pattern of distribution across the telencephalon. Medina et al., (2013) detected multi-cell structures consisting of a neuron enclosed by glial cells defined as perineuronal glial satellite cells (PGC) among Japanese jungle crow with increased numbers and sizes. On one side, the present study showed highly distributed clustered glial cells in the mesopallium and thalamus of the hooded crow (Corvus cornix) and in the hyperpallium and the nidopallium of chicken (Gallus gallus). On the other side, Medina et al., (2013) detected these satellite cells in the nidopallium caudalaterale of the New Caledonian crows in sparsely distributed

864 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613 forms and were clearly distinguished with high number of clustering in the mesopallium and the hyperpallium densocellulare area of Australian magpie, Indian mynah, and zebra finch and not in pigeons and chickens. Furthermore, our results agree with results of Medina et al., (2013) about the absence of perineuronal glial clustered cells in pigeons, but were contradictory concerning their distribution in chicken (Gallus gallus domesticus). Wild and confined New Caledonian crow (Corvus moneduloides) can construct new gears to encourage its entrance to food places through bowing fractions of wire to use as snares (Weir et al., 2002; Hunt and Gray, 2003). Our results suggested that their nominated activity of intelligent behavior and high cognitive abilities may be due to the distributed clustered glial cells in sub-regions of pallium including hyperpallium and the mesopallium. Although chickens and pigeons did not represent perinuclear glial cells in their hyperpallium and mesopallium, they form neural circuits important for audiovisual functions and passive avoidance (Nakamori et al., 2010; Town and McCabe, 2011), and color discrimination learning, respectively (Chaves and Hodos, 1997) Furthermore, the glycogen content widely distributed in hooded crows and may be functionally distributed to support the myelin sheath formation. Benzo and De Gennaro (1983) concluded that glycogen storage serves as a recyclable substrate for production of reducing equivalents that would be available for the myelin lipid cholesterol synthesis in the avian central nervous system. Additionally, Lyser (1973) observed that glycogen body cells considered as integral parts of CNS tissues and marked with an affinity for the astrocytes. Therefore, our results of the highly distributed glycogen content of hooded crow supported by the results of Suzuki et al. (2011) who explained that astrocytes and glial cells of the mammalian brain may play a vital role in converting glycogen to lactate and transporting it to neurons and through the breakdown of glycogen into glucose and regulate learning tasks. The present study findings were congruent with Rehkamper et al. (1991) who found that the slope of the canonical axis factor and hippocampus enlarged with 3.15 folds in passeriform than galliform. The distributed densely granular and fibrillar or non-fibrillar collagen in different brain regions of hooded crows (Corvus cornix) may be one of the main aspects triggering their higher cognitive memory abilities and intelligent behavior. Moreover, the main pallial areas including the hyperpallium, the mesopallium, and the nidopallium were recognized by their collagen granules and may be considered as one of the triggering factors boosting their cognitive memory and fine tool tasks abilities. Su et al. (2016) suggested that collagen acts as a synaptic triggering factor that may be diffusely localized in the developing mammalian cortex. Moreover, Su et al. (2016) found that matricryptin, (released from the non-fibrillar collagen XIX by plasmin cleavage (Oudart et al., 2015), were important to regulate the inhibitory nerve terminals formations of integrins signaling and their activity in the formation of cortical circuits of highly paracrine mechanisms regulating the synapses. Additionally, the depletion of non-fibrillar collagen XIX disrupts the formation of Parv+ inhibitory axosomatic synapses in the cerebral cortex (CTX) and triggering phenotypes associated with complex brain disorders. In the present study, hooded crows (Corvus cornix) expressed highly dense myelinated sheath axons in the nidopallium caudalaterale (NCL) with unique anatomical segmentation structure may have a valuable function for triggering their high cognitive memory and synaptic plasticity. The nidopallium of pigeon was with long distributed axons extended to the NCL region, which may be responsible for multiple sensory input limbic and motor output as explained by Güntürkün (2005) who identified that nidopallium caudalaterale in pigeons have dense innervation by dopaminergic fibers and are responsible for the cognitive brain behavior; while, the prefrontal cortex (PFC) in mammals is responsible for different cognitive behavior such as working memory reversal learning and reward prediction (Mogensen and Divac, 1993; Hartmann and Güntürkün, 1998; Diekamp et al., 2002; Rose and Colombo, 2005). Further, Butler et al., (2011) concluded that complex cognitive abilities are carried out through the endbrain in Aves and neocortex in mammals as both originated from the telencephalon area and evolved from the same structures in a common ancestor by convergent evolution. Moreover, Medina and Reiner, (2000) suggested that NCL and PFC are not genoarchitectonic homologous and independently evolved from different parts of the pallium, but are functionally analog (Jarvise et al., 2013; Chen et al., 2013; Miller and Cohen, 2001). Ditz and Nieder (2016) concluded that birds nidopallium caudalaterale (NCL) neurons can keep numerosities from one to thirty spots and display several qualities that are like that found in

865 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613 mammals and executed by the prefrontal cortex (PFC). Additionally, hippocampal formation is considered as the medial part of the pallium in both mammals and birds and considered as the major pallial segment of the limbic system required in spatial memory and learning functions (Bingman and Able, 2002). Our results revealed that the distribution of collagen in the cerebellum with its foliation was more than the pallial area. Iwaniuk et al. (2006) reported that birds resemble mammals in the morphological and anatomical features of the cerebellum as both have variable convoluted folded cerebellar areas more than amphibian and reptiles. Moreover, Butler and Hodos (2005) and Iwaniuk et al. (2009) suggested that increased cerebellar foliation increases the density of neural circuit allowing increased capacity and enhanced motor abilities and manipulating and tool use skills.

Conclusion

The results of the present study concluded that: 1) The perineuronal satellite glial cells, either clustered alone or enclosing the neuronal cell body may be important for increasing the neural transmission. Particularly, the visible nuclear chromatin mass in these cells suggested that the cells may correspond to oligodendrocytes and may play a major role in normal brain functions such as cognitive abilities of birds. 2) The highly distributed amounts of collagen in crow species and their unique anatomical structure of partitions in nidopallium caudalaterale (NCL) may shed light on their importance in triggering the cognitive behavior and intelligence. 3) On the basis of the promising findings presented in this study, complete studying the neural comparative structure of more avian species will be needed to verify the effective role of collagen and glycogen execute more intelligence tasks. Additionally, more experiments will be needed to verify our results using immunohistochemical and electrophysiological behavioral studies to elucidate the functional role of different neuroanatomical structures that have evolved with the emergeance of complex cognition learning skills or triggered by environmental needs.

Acknowledgment

The authors would like gratefully to thank Dr. Hesham Abdel Aziz, Lecturer of English Literature, Faculty of Arts, Beni Suef University, Egypt for his English revision and editing.

Disclosure of interests

The authors declare no conflicts of interest and they are alone responsible for manuscript writing and analysis.

References

Beckers, G.J., J. Van der Meij, and J.A. Lesku, 2014. Plumes of neuronal activity propagate in three dimensions through the nuclear avian brain. BMC Biology, 12, 16. Benzo, C.A. and L.D. De Gennaro, 1983. An hypothesis of function for the avian glycogen body: a novel role for glycogen in the central nervous system. Med. Hypotheses ,10, 69-76. Bingman, V.P. and K.P. Able, 2002. Maps in birds: representational mechanisms and neural bases. Curr. Opin. Neurobiol., 12, 745 -750. Butler, A.B., A. Reiner, and H.J. Karten, 2011. Evolution of the amniote pallium and the origins of mammalian neocortex. Ann NY Acad Sci, 1225, 14–27. Butler, A.B. and W. Hodos, 2005. Comparative vertebrate neuroanatomy, 2nd edn. New York, NY: Wiley-Liss. Chaves, L.M. and W. Hodos, 1997. Hyperstriatum ventrale in pigeons: effects of lesions on color- discrimination and color-reversal learning. Vis Neurosci,14, 1029–1041. Chen, C.C., C.M. Winkler, A.R. Pfenning, and E.D. Jarvis, 2013. Molecular profiling of the developing avian telencephalon: regional timing and brain subdivision continuities. J Comp Neurol, 521, 3666–3701.

866 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Cohen, Y.E., G.L. Miller, and E.I. Knudsen, 1998. Forebrain pathway for auditory space processing in the barn owl. J. Neurophys, 79, 891–902. De Gennaro, L.D. 1959. Differentiation of the glycogen body of the chick embryo under normal and experimental conditions. Growth 23: 235. Diekamp, B., A. Gagliardo, and O. Güntürkün, 2002. Nonspatial and subdivision-specific working memory deficits after selective lesions of the avian prefrontal cortex. J Neurosci 22, 9573–9580. Ditz, H.M., and A. Nieder, 2016). Sensory and Working Memory Representations of Small and Large Numerosities in the Crow Endbrain. J Neurosci, 47, 12044-12052. Doyle, W.L. and R.L. Watterson, 1949. The accumulation of glycogen in the "glycogen body" of the nerve cord of the developing chick. J Morphol, 85, 319. Evans. S.E., 2000. Evolutionary Developmental Biology of the Cerebral Cortex. (eds Bock, G. & Cardew, G.) 109–113 (John Wiley & Sons, ltd., 2000). Godfrey-Smith, P., 2001. Environmental complexity and the evolution of cognition. In: Sternberg R, Kaufman J, editors. The evolution of intelligence. Mahwah, New Jersey: Lawrence Erlbaum Associates London. pp.223–250. Güntürkün, O., 2005. The avian prefrontal cortex and cognition. Curr. Opin. Neurobiol., 15, 686–693. Hartmann, B. and O. Güntürkün, 1998. Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: possible behavioral equivalencies to the mammalian prefrontal system. Behav. Brain. Res., 9, 125–133. Hudson, B.G., K. Tryggvason, M. Sundaramoorthy, and E.G. Neilson, 2003. Alport’s syndrome, Goodpasture’s syndrome, and type IV collagen. N. Engl. J. Med., 348, 2543–2556. Hunt, G.R. and R.D. Gray, 2003. Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc. Biol. Sci., 270, 867–874. Hunt, G.R., 2000. Human-like, population-level specialization in the manufacture of pandanus tools by New Caledonian crows Corvus moneduloides. Proc. Biol. Sci., 267, 403–413. Iwaniuk, A.N., L. Lefebvre, and D.R. Wylie, 2006. The comparative approach and brain-behaviour relationships: a tool for understanding tool use. Can. J. Zool., 63, 150–159. Iwaniuk, A.N., S.L. Olson, and H.F. James, 2009. Extraordinary cranial specialization in a new genus of extinct duck (Aves: Anseriformes) from Kauai, Hawaiian Islands. Zootaxa, 47–67. Jarvis, E.D., J. Yu, M.V. Rivas, H. Horita, G. Feenders, O. Whitney, S.C. Jarvis, E.R. Jarvis, L. Kubikova, E.P. Puck, C. Siang-Bakshi, S. Martin, M. McElroy, E. Hara, J. Howard, A. Pfenning, H. Mouritsen, C.C. Chen, and K. Wada, 2013. Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J Comp Neurol, 521, 3614–3665. Jarvis, E.D., O. Güntürkün, L. Bruce, A. Csillag, H. Karten, W. Kuenzel, L. Medina, G. Paxinos, D.J. Perkel, T. Shimizu, G. Striedter, J.M. Wild, G.F. Ball, J. Dugas-Ford, S.E. Durand, G.E. Hough, S. Husband, L. Kubikova, D.W. Lee, C.V. Mello, A. Powers, C. Siang, T.V. Smulders, K. Wada, S.A. White, K. Yamamoto, J. Yu, A. Reiner, A.B. Butler, Avian Brain Nomenclature Consortium. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci., 6, 151–159. Jerison, H.J., 1985. Animal intelligence as encephalization. Philosophical Transactions of the Royal Society of London, 308, 21–35. Karten, H.J., 1969. The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. In: Petras J, editor. Comparative and evolutionary aspects of the vertebrate central nervous system, vol. 167. New York: Annals of the New York Academy of Sciences. PP. 146–179. Karten, H.J. and T. Shimizu, 1989. The origins of neocortex: connections and lamination as distinct events in evolution. J. Cog. Neurosci,1:291–301. Karten, H.J., 1991. Homology and evolutionary origins of the neocortex. Brain Behav. Evol., 38, 264–272. Kenward, B., C. Rutz, A.A.S. Weir, J. Chappell, and A. Kacelnik, 2004. Morphology and sexual dimorphism of the New Caledonian Crow Corvus moneduloides, with notes on its behavior and ecology. Ibis., 146, 652–660.

867 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Krushinsky, L.V., L.P. Dobrokhotova and E.G. Shkol’nikYarros, 19850. Elementary Rational Activity and Morphophysiological Parallels in the Forebrain of Birds and Mammals. Zh. Obshch. Biol., 46, 633–644. Ludders, J.W., 2008. Anesthesia and analgesia in birds. In: Fish RE, Brown MJ, Danneman PJ, Karas AZ, eds. Anesthesia and analgesia in laboratory animals. Amsterdam; Boston: Elsevier/Academic, 481–500. Luna, L.G., 1992. Histopathologic Methods and Color Atlas of Special Stains and Tissue Artifacts; American Histolabs Inc. PP. 439. Lyser, K.M., 1973. The fine structure of the glycogen body of the chicken. Acta Anat. 85, 533. Medin, F.S., G.R. Hunt, R.D. Gray, J.M. Wild and M.F. Kubke, 2013. Perineuronal satellite neuroglia in the telencephalon of New Caledonian crows and other Passeriformes: evidence of satellite glial cells in the central nervous system of healthy birds?. Peer J., 1, 110. Medina, L. and A. Reiner, 2000. Do birds possess homologes of mammalian primary visual, somatosensory and motor cortices?. Trends. Neurosci., 23, 1–12. Miller, E.K. and J.D. Cohen, 2001. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci., 24, 167–202. Mogensen, J. and I. Divac, 1993. Behavioural effects of ablation of the pigeon-equivalent of the mammalian prefrontal cortex. Behav. Brain. Res., 55, 101–107. Nakamori, T., K. Sato, Y. Atoji, T. Kanamatsu, K. Tanaka and H. Ohki-Hamazaki, 2010. Demonstration of a neural circuit critical for imprinting behavior in chicks. J. of Neurosci., 30, 4467–4480. Nauta, W.J. and H.J. Karten, 1970. A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. In: Schmitt FO, editor. The neurosciences: second study program. New York: Rockefeller University Press. PP. 7–26. Oudart, J.B., S. Brassart Pasco and A. Vautrin, 2015. Plasmin releases the anti-tumor peptide from the NC1 domain of collagen XIX. Oncotarget. 6, 3656–3668. Palmgren, A. 1948. A rapid method for selective silver staining of nerve fibers and nerve endings in mounted paraffin sections. Acta. Zool. Stockh., 29, 377. Pepperberg, I.M. 2002. The Alex studies. Cambridge, MA: Harvard University Press. Portmann, A. 1947. Etudes sur la cérébralisation des oiseaux. II. Les indices intra-cérébraux. Alauda15, 1–15. Puelles, L., E. Kuwana, E. Puelles, A. Bulfone, K. Shimamura, J. Keleher, S. Smiga, and J. Rubenstein, 2000. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol., 424, 409–438. Puelles, L., J.E. Sandoval, A. Ayad, R. Del Corral, A. Alonso, J.L. Ferran and Martınez-de-la-Torre, 2017. The Pallium in Reptiles and Birds in the Light of the Updated Tetrapartite Pallium Model. Evolution of Nervous Systems, 2nd edition, Volume 1. Ramont, L., S. Brassart-Pasco, J. Thevenard, A. Deshorgue, L. Venteo, J.Y. Laronze, M. Pluot, J.C. Monboisse and F.X. Maquart, 2007. The C1 domain of type XIX collagen inhibits in vivo melanoma growth. Mol. Cancer. Ther., 6, 506–514. Rehkämper, G., H.D. Frahm, and K. Zilles, 1991. Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (Insectivores and Primates). Brain. Behav. Evol., 37, 125-143. Reiner, A., D.J. Perkel, L.L. Bruce, A.B. Butler, A. Csillag, W. Kuenzel, L. Medina, G. Paxinos, T. Shimizu, G. Striedter, M. Wild, G.F. Ball, S. Durand, O. Gunturkun, D.W. Lee, D.W. Mello, C.V. Powers, A. White, S.A. Hough, G. Kubikova, L. Smulders, T.V. Wada, K. Dugas-Ford, J. Husband, S. Yamamoto, K. Yu, J. Siang, C. and Jarvis, E.D. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol., 473, 377–414 Rose, J. and M. Colombo, 2005. Neural correlates of executive control in the avian brain. PLoS. Biol., 3, 190. Roth, G., and U. Dicke, 2005. Evolution of the brain and intelligence. Trends in Cognitive Sci., 9, 250-257.

868 Middle East J. Appl. Sci., 7(4): 857-869, 2017 ISSN 2077-4613

Smith-Fernandez, A., C. Pieau, J. Reperant, E. Boncinelli, and M. Wassef, 1998. Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes. Develop., 125, 2099– 2111. Sterelny, K. 2003. Thought in a hostile world. In Blackwell. New York, NY. Su, J., R.S. Stenbjorn, K. Gorse, K. Su, K.F. Hauser, S. Ricard-Blum, T. Pihlajaniemi, and M.A. Fox, 2012. Target-derived matricryptins organize cerebellar synapse formation through α3β1 integrins. Cell. Rep., 2, 223–230. Su, J., J. Chen, K. Lippold, A. Monavarfeshani, G.L. Carrillo, R. Jenkins, and M.A. Fox, 2016. Collagen-derived matricryptins promote inhibitory nerve terminal formation in the developing neocortex. J. Cell Biol., 212, 721-736. Suzuki, A., S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti and C.M. Alberini, 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell, 144, 810–823. Thomas, B. and K. Kotrschal, 2004. Leading a conspecific away from food in ravens (Corvus Corax)?. Anim. Cogn., 7, 69–76. Thompson, S.W., 1966 Selected histochemical and histopathological methods, Charles C. Thomas, Springfield, IL. Town, S.M. and B.J. McCabe, 2011. Neuronal plasticity and multisensory integration in filial imprinting. PLoS One, 6, e17777. Wang, T., A.G. Hauswirth, A. Tong, D.K. Dickman, G.W. Davis, et al., 2014. Endostatin is a trans- synaptic signal for homeostatic synaptic plasticity. Neuron 83, 616–629. Weir, A.S., J. Chappell, and J. Kacelnik, 2002. Shaping of hooks in New Caledonian crows. Science., 297, 981. Zorina, Z.A., A.A. Smirnova, M.G. Pleskacheva and E.V. Dubynina, 2006. News in Studies on the Brain and Higher Nervous Activity of Corvid Birds (2002–2005), in (Ecology of Corvids in Natural and Anthropogenic Landscapes of Russia: Proc. All Russia Sci. Conf. on Studies of Corvid Birds), Kazan: Novoe Znanie pp. 16–43.

869