Abstract
Nissl and Golgi staining techniques have been employed to explore the neuronal subtypes in frontal lobe of Indian gray mongoose. A wide study of sixth layer in cerebral cortex of gyrencephalic and lissencephalic brains of mammals pointed out that pyramidal neurons are the dominant projection neuron in the cortical region and contribute to major neuronal circuitry. Frontal lobe well connected with other cortical and subcortical brain structures have been related with coordination of motor behaviour. Studies related to mammalian cortices focused mainly on pyramidal neurons, however, the details for other neuronal classes have gained less attention. Hence the aim of the present study was to explore different types of neuronal classes within frontal lobe of mongoose. Eleven types of neurons were identified in the mongoose frontal isocortex on the basis of morphology as seen in the Golgi-impregnated sections. Diversity of neuronal subtypes in frontal lobe of mongoose adds to the integration ability of sensory inputs and better processing. The specialized neuronal features observed in frontal lobe have been correlated with better decision making and attention skills thereby providing improved skills for prey and predator mode of action in mongoose.
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von Economo C (1927) Zellaufbau der Grosshirnrinde des Menschen: Zehn Vorlesungen. Julius Springer, Berlin
Tunturi AR (1971) Classification of neurons in the ectosylvian auditory cortex of the dog. J Comp Neurol 142:153–166
Gilbert CD, Kelly JP (1975) The projections of cells in different layers of the cat’s visual cortex. J Comp Neurol 163:81–106
Mitra NL (1955) Quantitative analysis of cell types in mammalian neo-cortex. J Anat 89:467–483
Garey LJ, Saini KD (1981) Golgi studies of the neuronal development of neurons in the lateral geniculate nucleus of the monkey. Exp Brain Res 44:117–128
Lund JS, Boothe Henry GH, Macqueen CL, Harvey AR (1979) Anatomical organization of the primary visual cortex area 171 of the cat. A comparison with area 17 of the macaque monkey. J Comp Neurol 184:599–618
Garey LJ, Winkelmann E, Brauer K (1985) Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. J Comp Neurol 240:305–321
Chagnac-Amitai Y, Luhmann HJ, Prince DA (1990) Burst generating and regular spiking layer V pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol 296:598–613
Eayrs JT, Goodhead B (1959) Postnatal development of the cerebral cortex in the rat. J Anat 93(4):385–402
Tyler CJ, Dunlop SA, Lund RD, Harman AM, Dann JF, Beazley LD, Lund JS (1998) Anatomical comparison of the macaque and marsupial visual cortex: common features that may reflect retention of essential cortical elements. J Comp Neurol 400:449–468
Fitzpatrick DC, Henson OW (1994) Cell types in mustached bat auditory cortex. Brain Behav Evol 43:79–91
Zervas M, Walkley SU (1999) Ferret pyramidal cell dendritogenesis: changes in morphology and ganglioside expression during cortical development. J Comp Neurol 413:429–448
Elston GN, Tweedale R, Rosa MGP (1999) Cellular heterogeneity in cerebral cortex. A study of the morphology of pyramidal neurones in visual areas of marmoset monkey. J Comp Neurol 415:33–51
Radtke-Schuller S (2001) Neuroarchitecture of the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). Anat Embryol 204:81–100
Hassiotis M, Ashwell KWS (2003) Neuronal classes in the isocortex of a monotreme, the Australian echidna (Tachyglossus aculeatus). Brain Behav Evol 61:6–27
Elston GN, Rockland KS (2002) The pyramidal cell of the sensori motor cortex of the macaque monkey: phenotypic variation. Cereb Cortex 12:1071–1078
Elston GN, Rosa MGP (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432–452
Elston GN, Tweedale R, Rosa MGP (1999) Cortical integration in the visual system of the macaque monkey: large scale morphological differences of pyramidal neurones in the occipital, parietal and temporal lobes. Proc R Soc Lond B Biol Sci 266:1367–1374
Jacobs B, Schall M, Prather M, Kapler L, Driscoll L, Baca S, Jacobs J, Ford K, Wainwright M, Treml M (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative study. Cereb Cortex 11:558–571
Lund JS, Yoshioka T, Levitt JB (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb Cortex 3:148–162
Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13:1124–1138
Elston GN, Benavides-Piccione R, DeFelipe J (2001) The pyramidal cell in cognition: a comparative study in human and monkey. J Neurosci 21(RC163):1–5
Hof PR, Glezer II, Condé F, Flagg R, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of calcium-binding proteins paravalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77–116
Nieuwenhuys R (1994) The Neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat Embryol 190:307–337
Srivastava UC, Singh S, Chauhan P (2013) Heterogeneity of spine density in pyramidal neurons of isocortex of mongoose, Herpestes edwardsii (É.Geoffroy Saint-Hilaire 1818). Microsc Res Tech 76:818–828
Peters A, Jones EG (1984) Classification of cortical neurons. In: Peters A, Jones EG (eds) Cellular components of the cerebral cortex, Cerebral cortex 1. Plenum, New York, pp 107–121
Muller LJ, Verwer RWH, Nunes Cardozo B, Vrensen G (1984) Synaptic characteristics of the identified pyramidal and multipolar non-pyramidal neurons in the visusal cortex of young and adult rabbits. A qualitative Golgi-electron microscope study. Neuroscience 12(4):1071–1087
Martini F (2007) Neural tissue and Neurophysiology. In: Martini FH (ed) Anatomy and physiology. Rex Bookstore Inc., Pearson Education South Asia Pte. Ltd, Jurong, Singapore, pp 284–316
Bruno C, Etienne A, Bertrand L, Maria CA, Nicole R, Keisuke T, Shaul H, Jean R (1997) Molecular and physiological diversity of cortical non-pyramidal cells. J Neurosci 17(10):3894–3906
Fuster JM (2002) Frontal lobe and cognitive development. J Neurocytol 31:373–385
Kawaguchi Y, Kubota Y (1995) Local circuit neurons in the frontal cortex and the neostriatum. In: Kimura M, Graybiel AM (eds) Functions of cortico-basal ganglia loop. Springer, Tokyo, pp 73–88
Blaesing B, Nossoll M, Teuchert Noodt G, Dawirs RR (2001) Postnatal maturation of prefrontal pyramidal neurons is sensitive to single early dose of methamphetamine in gerbil (Meriones unguiculatus). J Neural Trans 103:101–103
Valverde F (1970) The Golgi method, a tool for comparative structural analysis. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, New York, pp 12–31
Abbie AA (1940) Cortical lamination in the monotremata. J Comp Neurol 72:429–467
Ferrer I, Fabrigues I, Condom E (1986) A Golgi study of the sixth layer of the cerebral cortex. I. The lissencephalic brain of rodentia, lagomorpha, insectivora and chiroptera. J Anat 145:217–234
Valverde E, Facal-Valverde MV (1986) Neocortical layers I and II of the hedgehog (Erinaeus europaeus). I. Intrinsic organization. Anat Embryol 173:413–430
Galofré E, Ferrer I (1987) Development of dendritic spines in the Vth’s layer pyramidalneurons of rat’s somatosensory cortex. A qualitative and quantitative study with the Golgi method. J Hirnforsch 28:653–659
Mathers LH Jr (1979) Postnatal development in the rabbit visual cortex. Brain Res 168:21–29
Ferrer I, Fabrigues I, Condom E (1986) A Golgi study of the sixth layer of the cerebral cortex. II. The gyrencephalic brain of carnivora, artiodactyla and primates. J Anat 146:87–104
Sherwood CC, Lee PWH, Rivara CB, Holloway RL, Gilissen EPE, Simmons RMT, Hakeem A, Allman JM, Erwin JM, Hof PR (2003) Evolution of specialized pyramidal neurons in primate visual and motor cortex. Brain Behav Evol 61:28–44
Srivastava UC, Chand P, Maurya RC (2007) Cytoarchitectonic organization and morphology of the cells of hippocampal complex in strawberry finch (Estrilda amandava). Cell Mol Biol 53:103–120
Srivastava UC, Chand P, Maurya RC (2009) Neuronal classes in the corticoid complex of the telencephalon of the strawberry finch, Estrilda amandava. Cell Tissue Res 336:393–409
Tömböl T, Davies DC, Németh A, Sebestény T, Alpár A (2000) A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat Embryol 201:85–101
Srivastava UC, Singh S (2012) Seasonal plasticity in neurons of APH in female Indian ringneck parrot (Psittacula krameri). Nat Acad Sci Lett 35(4):259–262
Srivastava UC, Singh S, Singh D (2012) Seasonal fluctuation in the neuronal classes of Parahippocampal area of P. krameri (Scopoli, 1769) and E. scolopaceus (Linnaeus, 1758). Cell Mol Biol 58(Supp):OL1768–OL1779
Singh S, Singh D, Srivastava UC (2015) Seasonal dynamics within the neurons of hippocampus in adult female Indian ring neck parrot (Psittacula krameri) and Asian koel (Eudynamys scolopaceus). Can J Zool 93(3):157–175
Walsh TM, Ebner FF (1970) The cytoarchitecture of somatic sensory-motor cortex in the opossum (Didelphis marsupialis virginiana): a Golgi study. J Anat 107:1–18
Peters A, Regidor J (1981) A reassessment of the forms of non pyramidal neurons in cat visual cortex. J Comp Neurol 203:685–716
Simons DJ, Woolsey TA (1984) Morphology of Golgi-Cox impregnated barrel neurons in rat SmI cortex. J Comp Neurol 230:119–132
Jones EG (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160:205–267
Glezer II, Morgane PJ (1990) Ultrastructure of synapses and Golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale. Brain Res Bull 24:401–427
Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428
Somogyi P, Freund TF, Cowey A (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7:2577–2609
Armstrong C, Krook-Magnuson E, Soltesz I (2012) Neurogliaform and Ivy cells: a major family of nNOS expressing GABAergic neurons. Front Neural Circuits. doi:10.3389/fncir.2012.00023
Stuss DT, Gow CA, Hetherington CR (1992) ‘No longer Gage’: frontal lobe dysfunction and emotional changes. J Consult Clin Psychol 60:349–359
Acknowledgments
This research work is supported by Council of Scientific and Industrial Research (CSIR) JRF- fellowship (F. No.10-2(5)/2006(i)-E.U. II) granted to Mr. Prashant Chauhan. The authors thank the Head of Department of Zoology, University of Allahabad, Allahabad for providing essential facilities for the present investigation.
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Singh, S., Chauhan, P., Singh, D. et al. Distribution of Non-pyramidal Neurons in the Frontal Lobe of Indian Gray Mongoose (Herpestes edwardsii). Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 88, 209–217 (2018). https://doi.org/10.1007/s40011-016-0748-5
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DOI: https://doi.org/10.1007/s40011-016-0748-5