A Survey of White Matter Neurons at the Gyral Crowns and Sulcal Depths in the Rhesus Monkey

Gyrencephalic brains exhibit deformations of the six neocortical laminae at gyral crowns and sulcal depths, where the deeper layers are, respectively, expanded and compressed. The present study addresses: (1) the degree to which the underlying white matter neurons (WMNs) observe the same changes at gyral crowns and sulcal depths; and (2) whether these changes are consistent or variable across different cortical regions. WMNs were visualized by immunohistochemistry using the pan-neuronal label NeuN, and their density was quantified in eight rhesus monkey brains for four regions; namely, frontal (FR), superior frontal gyrus (SFG), parietal (Par) and temporal (TE). In all four regions, there were about 50% fewer WMNs in the sulcal depth, but there was also distinct variability from region to region. For the gyral crown, we observed an average density per 0.21 mm2 of 82 WMNs for the FR, 51 WMNs for SFG, 80 WMNs for Par and 93 WMNs for TE regions. By contrast, for the sulcal depth, the average number of WMNs per 0.21 mm2 was 41 for FR, 31 for cingulate sulcus (underlying the SFG), 54 for Par and 63 for TE cortical regions. Since at least some WMNs participate in cortical circuitry, these results raise the possibility of their differential influence on cortical circuitry in the overlying gyral and sulcal locations. The results also point to a possible role of WMNs in the differential vulnerability of gyral vs. sulcal regions in disease processes, and reinforce the increasing awareness of the WMNs as part of a complex, heterogeneous and structured microenvironment.

[1]  H. Gertz,et al.  Inhomogeneous distribution of Alzheimer pathology along the isocortical relief. Are cortical convolutions an Achilles heel of evolution? , 2017, Brain pathology.

[2]  Nadine C. Heyworth,et al.  Evaluation of Long-Term Cryostorage of Brain Tissue Sections for Quantitative Histochemistry , 2017, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[3]  Loren L Looger,et al.  Molecularly Defined Subplate Neurons Project Both to Thalamocortical Recipient Layers and Thalamus , 2016, Cerebral cortex.

[4]  Shantanu H. Joshi,et al.  Major Superficial White Matter Abnormalities in Huntington's Disease , 2016, Front. Neurosci..

[5]  V. Borrell,et al.  Cerebral cortex expansion and folding: what have we learned? , 2016, The EMBO journal.

[6]  Carlo Caltagirone,et al.  The superficial white matter in Alzheimer's disease , 2016, Human brain mapping.

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

[8]  John Seibyl,et al.  Partial-Volume Effect Correction Improves Quantitative Analysis of 18F-Florbetaben β-Amyloid PET Scans , 2016, The Journal of Nuclear Medicine.

[9]  M. E. Legidos-García,et al.  Prefrontal cortex afferents to the anterior temporal lobe in the Macaca fascicularis monkey , 2015, The Journal of comparative neurology.

[10]  G. Striedter,et al.  Cortical folding: when, where, how, and why? , 2015, Annual review of neuroscience.

[11]  David K. Yu,et al.  Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography , 2015, Proceedings of the National Academy of Sciences.

[12]  Camino de Juan Romero,et al.  Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly , 2015, The EMBO journal.

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

[14]  Jussi Tohka,et al.  Partial volume effect modeling for segmentation and tissue classification of brain magnetic resonance images: A review. , 2014, World journal of radiology.

[15]  K. Davis,et al.  Myelination, oligodendrocytes, and serious mental illness , 2014, Glia.

[16]  R. Hevner,et al.  Growth and folding of the mammalian cerebral cortex: from molecules to malformations , 2014, Nature Reviews Neuroscience.

[17]  M. Mesulam,et al.  Cholinergic circuitry of the human nucleus basalis and its fate in Alzheimer's disease , 2013, The Journal of comparative neurology.

[18]  Timothy D. Verstynen,et al.  Deterministic Diffusion Fiber Tracking Improved by Quantitative Anisotropy , 2013, PloS one.

[19]  W. Tseng,et al.  Sparse Solution of Fiber Orientation Distribution Function by Diffusion Decomposition , 2013, PloS one.

[20]  Goran Sedmak,et al.  The significance of the subplate for evolution and developmental plasticity of the human brain , 2013, Front. Hum. Neurosci..

[21]  W. Huttner,et al.  Conical expansion of the outer subventricular zone and the role of neocortical folding in evolution and development , 2013, Front. Hum. Neurosci..

[22]  Tuo Zhang,et al.  A functional model of cortical gyri and sulci , 2013, Brain Structure and Function.

[23]  Katrin Amunts,et al.  Development of cortical folding during evolution and ontogeny , 2013, Trends in Neurosciences.

[24]  C. Webber,et al.  Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia , 2013, Proceedings of the National Academy of Sciences.

[25]  A. McKee,et al.  The spectrum of disease in chronic traumatic encephalopathy. , 2013, Brain : a journal of neurology.

[26]  Dinggang Shen,et al.  Axonal fiber terminations concentrate on gyri. , 2012, Cerebral cortex.

[27]  C. Weickert,et al.  Higher Gamma-Aminobutyric Acid Neuron Density in the White Matter of Orbital Frontal Cortex in Schizophrenia , 2012, Biological Psychiatry.

[28]  D. Rosene,et al.  A stereological study of the numbers of neurons and glia in the primary visual cortex across the lifespan of male and female rhesus monkeys , 2012, The Journal of comparative neurology.

[29]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[30]  K. Rockland,et al.  Association of Type I Neurons Positive for NADPH-Diaphorase with Blood Vessels in the Adult Monkey Corpus Callosum , 2012, Front. Neural Circuits.

[31]  Z. Molnár,et al.  Morphology of mouse subplate cells with identified projection targets changes with age , 2012, The Journal of comparative neurology.

[32]  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.

[33]  Goran Sedmak,et al.  evelopmental history of the subplate zone , subplate neurons and interstitial hite matter neurons : relevance for schizophrenia , 2011 .

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

[35]  C. Weickert,et al.  Increased Interstitial White Matter Neuron Density in the Dorsolateral Prefrontal Cortex of People with Schizophrenia , 2011, Biological Psychiatry.

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

[37]  Heiko J Luhmann,et al.  The subplate and early cortical circuits. , 2010, Annual review of neuroscience.

[38]  Y. Yonekawa,et al.  Selective changes in GABAA receptor subtypes in white matter neurons of patients with focal epilepsy. , 2009, Brain : a journal of neurology.

[39]  Juan Torres-Reveron,et al.  The Changing Roles of Neurons in the Cortical Subplate , 2009, Front. Neuroanat..

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

[41]  Maurice Ptito,et al.  Neuronal reduction in frontal cortex of primates after prenatal alcohol exposure , 2009, Neuroreport.

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

[43]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[44]  Paul J. Harrison,et al.  Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis , 2003, Molecular Psychiatry.

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

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

[47]  D L Rosene,et al.  Feature article: are neurons lost from the primate cerebral cortex during normal aging? , 1998, Cerebral cortex.

[48]  M. Mesulam,et al.  Infracortical interstitial cells concurrently expressing m2-muscarinic receptors, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate-diaphorase in the human and monkey cerebral cortex , 1998, Neuroscience.

[49]  I. Kostović,et al.  Laminar distribution of neuropeptide Y‐immunoreactive neurons in human prefrontal cortex during development , 1997, The Journal of comparative neurology.

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

[51]  K. Rockland.  Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1) , 1996, The Journal of comparative neurology.

[52]  W. Welker.  Why Does Cerebral Cortex Fissure and Fold , 1990 .

[53]  C. Shatz,et al.  Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population , 1989, The Journal of comparative neurology.

[54]  P S Goldman-Rakic,et al.  Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys , 1988, The Journal of comparative neurology.

[55]  D. Rosene,et al.  A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[56]  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.

[57]  W. Welker,et al.  Why Does Cerebral Cortex Fissure and Fold ? A Review of Determinants of Gyri and Sulci , 2022 .