The distribution, number, and certain neurochemical identities of infracortical white matter neurons in a chimpanzee (Pan troglodytes) brain

We examined the number, distribution, and immunoreactivity of the infracortical white matter neuronal population, also termed white matter interstitial cells (WMICs), throughout the telencephalic white matter of an adult female chimpanzee. Staining for neuronal nuclear marker (NeuN) revealed WMICs throughout the infracortical white matter, these cells being most numerous and dense close to the inner border of cortical layer VI, decreasing significantly in density with depth in the white matter. Stereological analysis of NeuN‐immunopositive cells revealed an estimate of approximately 137.2 million WMICs within the infracortical white matter of the chimpanzee brain studied. Immunostaining revealed subpopulations of WMICs containing neuronal nitric oxide synthase (nNOS, approximately 14.4 million in number), calretinin (CR, approximately 16.7 million), very few WMICs containing parvalbumin (PV), and no calbindin‐immunopositive neurons. The nNOS, CR, and PV immunopositive WMICs, possibly all inhibitory neurons, represent approximately 22.6% of the total WMIC population. As the white matter is affected in many cognitive conditions, such as schizophrenia, autism, epilepsy, and also in neurodegenerative diseases, understanding these neurons across species is important for the translation of findings of neural dysfunction in animal models to humans. Furthermore, studies of WMICs in species such as apes provide a crucial phylogenetic context for understanding the evolution of these cell types in the human brain.

[1]  P. Balaram.  Review for "The distribution, number and certain neurochemical identities of infracortical white matter neurons in a chimpanzee ( Pan troglodytes ) brain" , 2021 .

[2]  J. Hutsler,et al.  Supernumerary neurons within the cerebral cortical subplate in autism spectrum disorders , 2021, Brain Research.

[3]  H. Luhmann,et al.  Transient cortical circuits match spontaneous and sensory-driven activity during development , 2020, Science.

[4]  David Kulp,et al.  Innovations present in the primate interneuron repertoire , 2020, Nature.

[5]  I. Kostović.  The enigmatic fetal subplate compartment forms an early tangential cortical nexus and provides the framework for construction of cortical connectivity , 2020, Progress in Neurobiology.

[6]  K. Rockland,et al.  Distribution, number, and certain neurochemical identities of infracortical white matter neurons in the brains of three megachiropteran bat species , 2020, The Journal of comparative neurology.

[7]  K. Kubo,et al.  Increased densities of white matter neurons as a cross‐disease feature of neuropsychiatric disorders , 2019, Psychiatry and clinical neurosciences.

[8]  G. Sedmak,et al.  The total number of white matter interstitial neurons in the human brain , 2019, Journal of anatomy.

[9]  R. Insausti,et al.  Postnatal Development of NPY and Somatostatin-28 Peptidergic Populations in the Human Angular Bundle , 2019, Front. Neuroanat..

[10]  K. Rockland,et al.  The distribution, number, and certain neurochemical identities of infracortical white matter neurons in a lar gibbon (Hylobates lar) brain , 2018, The Journal of comparative neurology.

[11]  Z. Molnár.  Cortical layer with no known function , 2018, The European journal of neuroscience.

[12]  Zachary T. Nolan,et al.  Subset of Cortical Layer 6b Neurons Selectively Innervates Higher Order Thalamic Nuclei in Mice , 2018, Cerebral cortex.

[13]  J. Colombo.  Cellular complexity in subcortical white matter: a distributed control circuit? , 2018, Brain Structure and Function.

[14]  K. Rockland,et al.  A Survey of White Matter Neurons at the Gyral Crowns and Sulcal Depths in the Rhesus Monkey , 2017, Front. Neuroanat..

[15]  I. Kostović,et al.  Secondary expansion of the transient subplate zone in the developing cerebrum of human and nonhuman primates , 2016, Proceedings of the National Academy of Sciences.

[16]  J. Siegel,et al.  Organization of the sleep‐related neural systems in the brain of the harbour porpoise (Phocoena phocoena) , 2016, The Journal of comparative neurology.

[17]  S. Herculano‐Houzel,et al.  Continued Growth of the Central Nervous System without Mandatory Addition of Neurons in the Nile Crocodile (Crocodylus niloticus) , 2016, Brain, Behavior and Evolution.

[18]  Douglas L. Rosene,et al.  White Matter Neurons in Young Adult and Aged Rhesus Monkey , 2016, Front. Neuroanat..

[19]  M. Casanova,et al.  Review: Cortical construction in autism spectrum disorder: columns, connectivity and the subplate , 2016, Neuropathology and applied neurobiology.

[20]  Jamie L. Reed,et al.  Cortical cell and neuron density estimates in one chimpanzee hemisphere , 2016, Proceedings of the National Academy of Sciences.

[21]  Z. Molnár,et al.  Development, evolution and pathology of neocortical subplate neurons , 2015, Nature Reviews Neuroscience.

[22]  Z. Petanjek,et al.  Neocortical calretinin neurons in primates: increase in proportion and microcircuitry structure , 2014, Front. Neuroanat..

[23]  C. Weickert,et al.  High White Matter Neuron Density with Elevated Cortical Cytokine Expression in Schizophrenia , 2014, Biological Psychiatry.

[24]  P. Barbaresi,et al.  Characterization of NO-producing neurons in the rat corpus callosum , 2014, Brain and behavior.

[25]  Helen Barbas,et al.  Parallel prefrontal pathways reach distinct excitatory and inhibitory systems in memory‐related rhinal cortices , 2013, The Journal of comparative neurology.

[26]  P. Manger,et al.  Distribution of parvalbumin, calbindin and calretinin containing neurons and terminal networks in relation to sleep associated nuclei in the brain of the giant Zambian mole-rat (Fukomys mechowii) , 2013, Journal of Chemical Neuroanatomy.

[27]  Z. Molnár,et al.  Molecular diversity of early-born subplate neurons. , 2013, Cerebral cortex.

[28]  P. Clavenzani,et al.  Neurochemical features of boar lumbosacral dorsal root ganglion neurons and characterization of sensory neurons innervating the urinary bladder trigone , 2013, The Journal of comparative neurology.

[29]  H. Monyer,et al.  5-HT3A Receptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks , 2011, The Journal of Neuroscience.

[30]  Jon H. Kaas,et al.  Updated Neuronal Scaling Rules for the Brains of Glires (Rodents/Lagomorphs) , 2011, Brain, Behavior and Evolution.

[31]  C. Connor,et al.  White matter neuron alterations in schizophrenia and related disorders , 2011, International Journal of Developmental Neuroscience.

[32]  R. Anadón,et al.  Distribution of glycine immunoreactivity in the brain of the Siberian sturgeon (Acipenser baeri): Comparison with γ‐aminobutyric acid , 2011, The Journal of comparative neurology.

[33]  J. Brandstätter,et al.  SNAP25 expression in mammalian retinal horizontal cells , 2011, The Journal of comparative neurology.

[34]  B. Cauli,et al.  Activation of cortical interneurons during sleep: an anatomical link to homeostatic sleep regulation? , 2011, Trends in Neurosciences.

[35]  J. DeFelipe,et al.  Differential distribution of neurons in the gyral white matter of the human cerebral cortex , 2010, The Journal of comparative neurology.

[36]  N. Jovanov-Milošević,et al.  Populations of subplate and interstitial neurons in fetal and adult human telencephalon , 2010, Journal of anatomy.

[37]  J. Kaas,et al.  Cellular Scaling Rules for the Brains of an Extended Number of Primate Species , 2010, Brain, Behavior and Evolution.

[38]  P. Hof,et al.  Inhibitory interneurons of the human prefrontal cortex display conserved evolution of the phenotype and related genes , 2010, Proceedings of the Royal Society B: Biological Sciences.

[39]  Karl Zilles,et al.  Frontal White Matter Volume Is Associated with Brain Enlargement and Higher Structural Connectivity in Anthropoid Primates , 2010, PloS one.

[40]  R. Nagarajan,et al.  Cross-Species Analyses of the Cortical GABAergic and Subplate Neural Populations , 2009, Frontiers in neuroanatomy.

[41]  Diana K. Sarko,et al.  Neuroanatomy Original Research Article Cellular Scaling Rules of Insectivore Brains , 2022 .

[42]  G. Meyer,et al.  Neurons in the White Matter of the Adult Human Neocortex , 2009, Front. Neuroanat..

[43]  P. Manger,et al.  Acquisition of brains from the African elephant (Loxodonta africana): Perfusion-fixation and dissection , 2009, Journal of Neuroscience Methods.

[44]  D. Amaral,et al.  Neuroanatomy of autism , 2008, Trends in Neurosciences.

[45]  Kathleen S Rockland,et al.  Long‐distance corticocortical GABAergic neurons in the adult monkey white and gray matter , 2007, The Journal of comparative neurology.

[46]  Juan Torres-Reveron,et al.  Properties of Persistent Postnatal Cortical Subplate Neurons , 2007, The Journal of Neuroscience.

[47]  P. Hof,et al.  Scaling of Inhibitory Interneurons in Areas V1 and V2 of Anthropoid Primates as Revealed by Calcium-Binding Protein Immunohistochemistry , 2006, Brain, Behavior and Evolution.

[48]  S. Herculano‐Houzel,et al.  Cellular scaling rules for rodent brains , 2006, Proceedings of the National Academy of Sciences.

[49]  Patrick R Hof,et al.  Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[50]  P. Schoenemann,et al.  Prefrontal white matter volume is disproportionately larger in humans than in other primates , 2005, Nature Neuroscience.

[51]  I. Gritti,et al.  Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat , 2003, The Journal of comparative neurology.

[52]  B. Clancy,et al.  Structure and projections of white matter neurons in the postnatal rat visual cortex , 2001, The Journal of comparative neurology.

[53]  R. Reep.  Cortical Layer VII and Persistent Subplate Cells in Mammalian Brains , 2000, Brain, Behavior and Evolution.

[54]  H. Kennedy,et al.  Non-uniformity of neocortex: areal heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. , 2000, Cerebral cortex.

[55]  E. G. Jones,et al.  Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. , 1996, Archives of general psychiatry.

[56]  Paul Leonard Gabbott,et al.  Localisation of NADPH diaphorase activity and NOS immunoreactivity in astroglia in normal adult rat brain , 1996, Brain Research.

[57]  J. Hornung,et al.  Distribution of GABA-containing neurons in human frontal cortex: a quantitative immunocytochemical study , 1994, Anatomy and Embryology.

[58]  H. Gundersen,et al.  Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator , 1991, The Anatomical record.

[59]  P. Rakić,et al.  Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain , 1990, The Journal of comparative neurology.

[60]  C. Shatz,et al.  The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  H J Gundersen,et al.  The nucleator , 1988, Journal of microscopy.

[62]  M. Beal,et al.  Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: Normal anatomy and alterations in alzheimer's disease , 1988, Annals of neurology.

[63]  C. Shatz,et al.  Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  Pasko Rakic,et al.  Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon , 1980, Journal of neurocytology.

[65]  M. Bertelsen.  Issues Surrounding Surplus Animals in Zoos , 2019, Fowler's Zoo and Wild Animal Medicine Current Therapy, Volume 9.

[66]  G. Fishell,et al.  Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons , 2011, Developmental neurobiology.

[67]  P. Wahle,et al.  Morphology of neurons in the white matter of the adult human neocortex , 2005, Experimental Brain Research.

[68]  C. Beasley,et al.  Density and distribution of white matter neurons in schizophrenia, bipolar disorder and major depressive disorder: no evidence for abnormalities of neuronal migration , 2002, Molecular Psychiatry.

[69]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

[70]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[71]  F. Gallyas.  Silver staining of myelin by means of physical development. , 1979, Neurological research.