Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex.

In the primate neocortex, little is known about the possible associations between functional subclasses of GABA neurons, their morphological properties and calcium-binding protein (CaBP) content. We used whole-cell current clamp recordings, combined with intracellular labeling and fluorescence immunohistochemistry, to determine these relationships for interneurons in layers 2-3 of monkey prefrontal cortex (PFC). Eighty-one interneurons were included in the analysis. Thirty-eight of these cells showed immunoreactivity for one of the three CaBPs tested. Co-localization of more than one CaBP was not observed in any of the interneurons examined. Interneurons with different CaBPs formed distinct populations with specific physiological membrane properties and morphological features. Parvalbumin (PV)-positive cells had the physiological properties characteristic of fast-spiking interneurons (FS) and the morphology of basket or chandelier neurons. Most calretinin (CR)-containing cells had the physiological properties ascribed to non-fast-spiking cells (non-FS) and a vertically oriented axonal morphology, similar to that of double bouquet cells. Calbindin (CB)-positive interneurons also had non-FS properties and included cells with double bouquet morphology or with a characteristic dense web of axonal collaterals in layer 1. Classification of the interneurons based on cluster analysis of multiple electrophysiological properties suggested the existence of at least two distinct groups of interneurons. The first group contained mainly PV-positive FS cells and the second group consisted predominantly of CR- and CB-positive non-FS interneurons. These findings may help to illuminate the functional roles of different groups of interneurons in primate PFC circuitry.

[1]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[2]  K. Baimbridge,et al.  Calcium-binding proteins in the nervous system , 1992, Trends in Neurosciences.

[3]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[4]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[5]  D. Schmechel,et al.  Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory‐motor cortex , 1985, The Journal of comparative neurology.

[6]  P. Goldman-Rakic,et al.  Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[8]  Alex M Thomson,et al.  Physiological and morphological diversity of immunocytochemically defined parvalbumin‐ and cholecystokinin‐positive interneurones in CA1 of the adult rat hippocampus , 2002, The Journal of comparative neurology.

[9]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[10]  F. Karube,et al.  Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes , 2004, The Journal of Neuroscience.

[11]  J. Rossier,et al.  Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex , 1998, The European journal of neuroscience.

[12]  P. Goldman-Rakic,et al.  Destruction and Creation of Spatial Tuning by Disinhibition: GABAA Blockade of Prefrontal Cortical Neurons Engaged by Working Memory , 2000, The Journal of Neuroscience.

[13]  M. Celio,et al.  Intracellular concentration of parvalbumin in nerve cells , 1993, Brain Research.

[14]  Paul Leonard Gabbott,et al.  Vasoactive intestinal polypeptide containing neurones in monkey medial prefrontal cortex (mPFC): colocalisation with calretinin , 1997, Brain Research.

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

[16]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

[17]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[19]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[20]  A. Sampson,et al.  Gene Expression Deficits in a Subclass of GABA Neurons in the Prefrontal Cortex of Subjects with Schizophrenia , 2003, The Journal of Neuroscience.

[21]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[22]  A. Hendrickson,et al.  Developmental changes in calretinin expression in GABAergic and nonGABAergic neurons in monkey striate cortex , 1995, The Journal of comparative neurology.

[23]  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.

[24]  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.

[25]  Chris J. McBain,et al.  Interneurons unbound , 2001, Nature Reviews Neuroscience.

[26]  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.

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

[28]  J. Pierri,et al.  Altered GABA neurotransmission and prefrontal cortical dysfunction in schizophrenia , 1999, Biological Psychiatry.

[29]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[30]  Peter Somogyi,et al.  Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro , 2000, The Journal of physiology.

[31]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

[32]  Y. Kubota,et al.  Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. , 1993, Journal of neurophysiology.

[33]  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.

[34]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[35]  S. Hestrin,et al.  Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Paul Leonard Gabbott,et al.  Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics , 1996, The Journal of comparative neurology.

[37]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  H. Monyer,et al.  Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons , 2000, The Journal of Neuroscience.

[39]  David A Lewis,et al.  Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons. , 2003, Cerebral cortex.

[40]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[41]  J. Lund,et al.  Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin‐releasing factor‐and parvalbumin‐immunoreactive populations , 1990, The Journal of comparative neurology.

[42]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[43]  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.

[44]  Françoise Condé,et al.  Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology , 1994, The Journal of comparative neurology.

[45]  Egidio D'Angelo,et al.  Altered Neuronal Excitability in Cerebellar Granule Cells of Mice Lacking Calretinin , 2003, The Journal of Neuroscience.

[46]  P. Goldman-Rakic,et al.  Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. , 1999, Journal of neurophysiology.

[47]  V. Meskenaite,et al.  Calretinin‐immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis , 1997, The Journal of comparative neurology.

[48]  Charles E. Heckler,et al.  Applied Multivariate Statistical Analysis , 2005, Technometrics.

[49]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[51]  T. Preuss Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[52]  T. Sawaguchi,et al.  Delayed response deficits produced by local injection of bicuculline into the dorsolateral prefrontal cortex in Japanese macaque monkeys , 2004, Experimental Brain Research.

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

[54]  Orlando J. Castejón,et al.  The Basket Cells , 2003 .

[55]  M. Whittington,et al.  A Novel Network of Multipolar Bursting Interneurons Generates Theta Frequency Oscillations in Neocortex , 2003, Neuron.

[56]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[57]  C C Hilgetag,et al.  Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. , 2001, Cerebral cortex.

[58]  David A Lewis,et al.  Synaptic efficacy during repetitive activation of excitatory inputs in primate dorsolateral prefrontal cortex. , 2004, Cerebral cortex.

[59]  T. Sawaguchi,et al.  Delayed response deficit in monkeys by locally disturbed prefrontal neuronal activity by bicuculline , 1988, Behavioural Brain Research.

[60]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

[61]  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.

[62]  J. Fuster The Prefrontal Cortex , 1997 .

[63]  D. Lewis,et al.  Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. , 2000, Cerebral cortex.