Scaling of Inhibitory Interneurons in Areas V1 and V2 of Anthropoid Primates as Revealed by Calcium-Binding Protein Immunohistochemistry

Inhibitory GABAergic interneurons are important for shaping patterns of activity in neocortical networks. We examined the distributions of inhibitory interneuron subtypes in layer II/III of areas V1 and V2 in 18 genera of anthropoid primates including New World monkeys, Old World monkeys, and hominoids (apes and humans). Interneuron subtypes were identified by immunohistochemical staining for calbindin, calretinin, and parvalbumin and densities were quantified using the optical disector method. In both V1 and V2, calbindin-immunoreactive neuron density decreased disproportionately with decreasing total neuronal density. Thus, V1 and V2 of hominoids were occupied by a smaller percentage of calbindin-immunoreactive interneurons compared to monkeys who have greater overall neuronal densities. At the transition from V1 to V2 across all individuals, we found a tendency for increased percentages of calbindin-immunoreactive multipolar cells and calretinin-immunoreactive interneurons. In addition, parvalbumin-immunoreactive cell soma volumes increased from V1 to V2. These findings suggest that modifications of specific aspects of inhibition might be critical to establishing the receptive field properties that distinguish visual areas. Furthermore, these results show that phylogenetic variation exists in the microcircuitry of visual cortex that could have general implications for sensory processing.

[1]  P. Hof,et al.  The Evolution of Neuron Types and Cortical Histology in Apes and Humans , 2007 .

[2]  J. Kaas,et al.  Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[3]  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.

[4]  Derek E Wildman,et al.  Moving primate genomics beyond the chimpanzee genome. , 2005, Trends in genetics : TIG.

[5]  J. Hutsler,et al.  Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species , 2005, Brain Research.

[6]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[7]  Javier DeFelipe,et al.  Double bouquet cell in the human cerebral cortex and a comparison with other mammals , 2005, The Journal of comparative neurology.

[8]  J. Kaas The future of mapping sensory cortex in primates: three of many remaining issues , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  Jon H. Kaas,et al.  Regional Specialization in Pyramidal Cell Structure in the Visual Cortex of the Galago: An Intracellular Injection Study of Striate and Extrastriate Areas with Comparative Notes on New World and Old World Monkeys , 2005, Brain, Behavior and Evolution.

[10]  M. Gamberini,et al.  Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[11]  A. Schleicher,et al.  Transmitter receptors and functional anatomy of the cerebral cortex , 2004, Journal of anatomy.

[12]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[13]  G. Boynton,et al.  Visual Cortex: The Continuing Puzzle of Area V2 , 2004, Current Biology.

[14]  S. Anderson,et al.  Origins of Cortical Interneuron Subtypes , 2004, The Journal of Neuroscience.

[15]  P. Wahle,et al.  Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an Early period of postnatal development. , 2004, Cerebral cortex.

[16]  Karl Zilles,et al.  Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans , 2004, Brain, Behavior and Evolution.

[17]  D. Melnick,et al.  Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). , 2004, Journal of human evolution.

[18]  C. Andressen,et al.  Calcium-binding proteins: selective markers of nerve cells , 1993, Cell and Tissue Research.

[19]  T. Tsumoto,et al.  Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition , 1979, Experimental Brain Research.

[20]  E. G. Jones,et al.  Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities , 2004, Experimental Brain Research.

[21]  G. Elston Pyramidal cell heterogeneity in the visual cortex of the nocturnal new world owl monkey (aotus trivirgatus) , 2003, Neuroscience.

[22]  Tai Sing Lee,et al.  Computations in the early visual cortex , 2003, Journal of Physiology-Paris.

[23]  Chet C. Sherwood,et al.  Evolution of Specialized Pyramidal Neurons in Primate Visual and Motor Cortex , 2003, Brain, Behavior and Evolution.

[24]  R. S. Waters,et al.  Removal of GABAergic inhibition alters subthreshold input in neurons in forepaw barrel subfield (FBS) in rat first somatosensory cortex (SI) after digit stimulation , 2002, Experimental Brain Research.

[25]  Todd M Preuss,et al.  Human-specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. , 2002, Cerebral cortex.

[26]  P. Rakic,et al.  Origin of GABAergic neurons in the human neocortex , 2002, Nature.

[27]  N. Weber,et al.  Common Slope Tests for Bivariate Errors‐in‐Variables Models , 2002 .

[28]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

[29]  Peter R. Mouton,et al.  Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists , 2002 .

[30]  J R Nyengaard,et al.  Tissue shrinkage and unbiased stereological estimation of particle number and size * , 2001, Journal of microscopy.

[31]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[32]  Mark A. Changizi,et al.  Principles underlying mammalian neocortical scaling , 2001, Biological Cybernetics.

[33]  C. Nunn,et al.  Comparative methods for studying primate adaptation and allometry , 2001 .

[34]  Patrick R Hof,et al.  Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach , 2000, Journal of Chemical Neuroanatomy.

[35]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

[36]  T. Preuss Taking the Measure of Diversity: Comparative Alternatives to the Model-Animal Paradigm in Cortical Neuroscience , 2000, Brain, Behavior and Evolution.

[37]  Richard J. Salvi,et al.  GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex. , 2000, Neuroreport.

[38]  Anthony R. Ives,et al.  Using the Past to Predict the Present: Confidence Intervals for Regression Equations in Phylogenetic Comparative Methods , 2000, The American Naturalist.

[39]  Keiji Tanaka,et al.  Neurochemical gradients along monkey sensory cortical pathways: calbindin‐immunoreactive pyramidal neurons in layers II and III , 1999, The European journal of neuroscience.

[40]  J. Kaas,et al.  Distinctive compartmental organization of human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  G. Elston,et al.  Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey , 1999, The Journal of comparative neurology.

[42]  T. Insel,et al.  The primate neocortex in comparative perspective using magnetic resonance imaging. , 1999, Journal of human evolution.

[43]  L. Krubitzer,et al.  The evolution of visual cortex: where is V2? , 1999, Trends in Neurosciences.

[44]  Anthony R. Ives,et al.  An Introduction to Phylogenetically Based Statistical Methods, with a New Method for Confidence Intervals on Ancestral Values , 1999 .

[45]  P. Hof,et al.  Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns , 1999, Journal of Chemical Neuroanatomy.

[46]  Konrad Sandau,et al.  Unbiased Stereology. Three‐Dimensional Measurement in Microscopy. , 1999 .

[47]  A. Purvis,et al.  Comparative Primate Socioecology: Phylogenetically independent comparisons and primate phylogeny , 1999 .

[48]  F. Gage,et al.  Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. , 1999, The Journal of comparative neurology.

[49]  K Zilles,et al.  Limbic frontal cortex in hominoids: a comparative study of area 13. , 1998, American journal of physical anthropology.

[50]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

[51]  J. Morrison,et al.  Chapter II Neurochemical organization of the primate visual cortex , 1998 .

[52]  J. DeFelipe Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex , 1997, Journal of Chemical Neuroanatomy.

[53]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[54]  Javier DeFelipe,et al.  Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities , 1997, Journal of Chemical Neuroanatomy.

[55]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

[56]  G. Leuba,et al.  Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures , 1997, Journal of Chemical Neuroanatomy.

[57]  A. Burkhalter,et al.  Three distinct families of GABAergic neurons in rat visual cortex. , 1997, Cerebral cortex.

[58]  Paul Leonard Gabbott,et al.  Calretinin neurons in human medial prefrontal cortex (areas 24a,b,c, 32′, and 25) , 1997, The Journal of comparative neurology.

[59]  T. Price,et al.  Correlated evolution and independent contrasts. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[60]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[61]  Javier DeFelipe,et al.  Colocalization of parvalbumin and calbindin D-28k in neurons including chandelier cells of the human temporal neocortex , 1997, Journal of Chemical Neuroanatomy.

[62]  Paul Leonard Gabbott,et al.  Local‐circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution , 1997, The Journal of comparative neurology.

[63]  J. Prothero,et al.  Scaling of cortical neuron density and white matter volume in mammals. , 1997, Journal fur Hirnforschung.

[64]  M G Rosa,et al.  Comparison of dendritic fields of layer III pyramidal neurons in striate and extrastriate visual areas of the marmoset: a Lucifer yellow intracellular injection. , 1996, Cerebral cortex.

[65]  J. DeFelipe,et al.  Colocalization of calbindin D‐28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex , 1996, The Journal of comparative neurology.

[66]  S. Hendry,et al.  Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. , 1996, Cerebral cortex.

[67]  Paul Leonard Gabbott,et al.  Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions , 1996, The Journal of comparative neurology.

[68]  Todd M. Preuss,et al.  Cytochrome oxidase 'blobs' and other characteristics of primary visual cortex in a lemuroid primate, Cheirogaleus medius. , 1996, Brain, behavior and evolution.

[69]  H. Tamura,et al.  Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque. , 1995, Journal of neurophysiology.

[70]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[71]  E G Jones,et al.  Neurochemical gradient along the monkey occipito-temporal cortical pathway. , 1994, Neuroreport.

[72]  Kathleen S. Rockland,et al.  Primary Visual Cortex in Primates , 1994, Cerebral Cortex.

[73]  R K Carder,et al.  Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species , 1993, Visual Neuroscience.

[74]  P. Morgane,et al.  Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. , 1993, Cerebral cortex.

[75]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[76]  J. Lund,et al.  Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics , 1993, The Journal of comparative neurology.

[77]  Y. Kubota,et al.  Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex , 1993, Brain Research.

[78]  M. Pagel A method for the analysis of comparative data , 1992 .

[79]  R. Douglas,et al.  Exploring cortical microcircuits: a combined anatomical, physiological, and computational approach , 1992 .

[80]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[81]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[82]  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.

[83]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[84]  A. Hendrickson,et al.  Calcium‐binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex , 1990, The Journal of comparative neurology.

[85]  P H Harvey,et al.  Comparing brains. , 1990, Science.

[86]  E. G. Jones,et al.  Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity , 1989, Brain Research.

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

[88]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

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

[90]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

[91]  D. B. Tower,et al.  THE ACTIVITIES OF BUTYRYLCHOLINESTERASE AND CARBONIC ANHYDRASE, THE RATE OF ANAEROBIC GLYCOLYSTS, AND THE QUESTION OF A CONSTANT DENSITY OF GLIAL CELLS IN CEREBRAL CORTICES OF VARIOUS MAMMALIAN SPECIES FROM MOUSE TO WHALE , 1973, Journal of neurochemistry.

[92]  J. Kaas,et al.  Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[93]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[94]  R. Hassler Comparative Anatomy of the Central Visual Systems in Day- and Night-active Primates , 1966 .

[95]  D. B. Tower,et al.  Structural and functional organization of mammalian cerebral cortex: The correlation of neurone density with brain size. Cortical neurone density in the fin whale (Balaenoptera Physalus L.) with a note on the cortical neurone density in the Indian elephant , 1954, The Journal of comparative neurology.

[96]  W. E. Clark,et al.  The Visual Cortex of Primates. , 1925, Journal of anatomy.

[97]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .