Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates.

The prefrontal cortex selects relevant signals and suppresses irrelevant stimuli for a given task through mechanisms that are not understood. We addressed this issue using as a model system the pathways from the functionally distinct prefrontal areas 10 and 32 to auditory association cortex, and investigated their relationship to inhibitory neurons labeled for calbindin (CB) or parvalbumin (PV), which differ in mode of inhibition. Projection neurons in area 10 originated mostly in layers 2-3 and were intermingled with CB inhibitory neurons. In contrast, projections from area 32 originated predominantly in layers 5-6 among PV inhibitory neurons. Prefrontal axonal boutons terminating in layers 2-3 of auditory association cortex were larger than those terminating in layer 1. Most prefrontal axons synapsed on spines of excitatory neurons but a significant number targeted dendritic shafts of inhibitory neurons. Axons from area 10 targeted CB and PV inhibitory neurons, whereas axons from area 32 targeted PV inhibitory neurons. The preferential association of the 2 prefrontal pathways with distinct classes of inhibitory neurons at their origin and termination may reflect the specialization of area 10 in working memory functions and area 32 in emotional communication. These findings suggest diversity in inhibitory control by distinct prefrontal pathways.

[1]  J. Fiala,et al.  Cylindrical diameters method for calibrating section thickness in serial electron microscopy , 2001, Journal of microscopy.

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

[3]  P. Kalus,et al.  Altered distribution of parvalbumin-immunoreactive local circuit neurons in the anterior cingulate cortex of schizophrenic patients , 1997, Psychiatry Research: Neuroimaging.

[4]  P. Kalus,et al.  Inhibitory cartridge synapses in the anterior cingulate cortex of schizophrenics , 1999, Journal of Neural Transmission.

[5]  R. Demaree,et al.  Microwave Techniques and Protocols , 2001, Humana Press.

[6]  R. Knight,et al.  Prefrontal cortex regulates inhibition and excitation in distributed neural networks. , 1999, Acta psychologica.

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

[8]  A. Zaitsev,et al.  Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. , 2005, Cerebral cortex.

[9]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. II. Development of electrophysiological properties , 1994, The Journal of comparative neurology.

[10]  H. Barbas,et al.  Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure , 2006, The European journal of neuroscience.

[11]  K. Harris,et al.  Preservation of neuronal ultrastructure in hippocampal slices using rapid microwave-enhanced fixation , 1989, Journal of Neuroscience Methods.

[12]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[13]  J C Fiala,et al.  Reconstruct: a free editor for serial section microscopy , 2005, Journal of microscopy.

[14]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[15]  M. L. Pucak,et al.  Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex , 1998, The Journal of comparative neurology.

[16]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[17]  M. Petrides.  Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[19]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Henry Markram,et al.  Synaptic pathways in neural microcircuits , 2005, Trends in Neurosciences.

[21]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[22]  R. Murray,et al.  The Neural Correlates of Inner Speech and Auditory Verbal Imagery in Schizophrenia: Relationship to Auditory Verbal Hallucinations , 1996, British Journal of Psychiatry.

[23]  F. Benes,et al.  The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects , 2001, Biological Psychiatry.

[24]  R. Parasuraman.  The attentive brain , 1998 .

[25]  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.

[26]  H. Barbas,et al.  Prefrontal Projections to the Thalamic Reticular Nucleus form a Unique Circuit for Attentional Mechanisms , 2006, The Journal of Neuroscience.

[27]  M. Carpenter.  The Fine Structure of the Nervous System , 1970, Neurology.

[28]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[29]  P. Goldman-Rakic,et al.  Prefrontal Microcircuits: Membrane Properties and Excitatory Input of Local, Medium, and Wide Arbor Interneurons , 2001, The Journal of Neuroscience.

[30]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[31]  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.

[32]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[33]  David A. Lewis,et al.  Impaired prefrontal inhibition in schizophrenia: relevance for cognitive dysfunction , 2002, Physiology & Behavior.

[34]  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.

[35]  D. Melchitzky,et al.  Synaptic targets of calretinin-containing axon terminals in macaque monkey prefrontal cortex , 2005, Neuroscience.

[36]  F. Benes,et al.  GABAergic Interneurons: Implications for Understanding Schizophrenia and Bipolar Disorder , 2001, Neuropsychopharmacology.

[37]  H. Barbas.  Pattern in the cortical distribution of prefrontally directed neurons with divergent axons in the rhesus monkey. , 1995, Cerebral cortex.

[38]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[39]  Diego Contreras,et al.  Electrophysiological classes of neocortical neurons , 2004, Neural Networks.

[40]  A. Burkhalter,et al.  Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex. , 1999, Cerebral cortex.

[41]  H. Barbas,et al.  Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression , 2003, BMC Neuroscience.

[42]  J. D. Newman,et al.  Anatomical and physiological evidence for a relationship between the ‘cingular’ vocalization area and the auditory cortex in the squirrel monkey , 1980, Brain Research.

[43]  R. O’Reilly,et al.  A computational approach to prefrontal cortex, cognitive control and schizophrenia: recent developments and current challenges. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[44]  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.

[45]  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.

[46]  C. Beasley,et al.  The density and spatial distribution of gabaergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia , 2002, Biological Psychiatry.

[47]  E. G. Jones,et al.  A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons , 1990, Neuroscience.

[48]  A. Reiner,et al.  Pathway tracing using biotinylated dextran amines , 2000, Journal of Neuroscience Methods.

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

[50]  E. White.  Cortical Circuits , 1989, Birkhäuser Boston.

[51]  J. Deuchars,et al.  Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. , 1997, Cerebral cortex.

[52]  C. Beasley,et al.  Neurochemical correlates of cortical GABAergic deficits in schizophrenia: selective losses of calcium binding protein immunoreactivity , 2001, Brain Research Bulletin.

[53]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[54]  R. Dolan,et al.  The role of the prefrontal cortex in higher cognitive functions. , 1996, Brain research. Cognitive brain research.

[55]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[56]  A. Peters,et al.  The organization of double bouquet cells in monkey striate cortex , 1997, Journal of neurocytology.

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

[58]  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.

[59]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[60]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of response modality and processing domain. , 2001, Cerebral Cortex.

[61]  C. Beasley,et al.  Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics , 1997, Schizophrenia Research.

[62]  H. Barbas,et al.  Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. , 2005, Cerebral cortex.

[63]  E G Jones,et al.  Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[64]  S. Sesack,et al.  Axosomatic input to subpopulations of cortically projecting pyramidal neurons in primate prefrontal cortex , 1997, Synapse.

[65]  Karl J. Friston,et al.  Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia , 1995, Nature.

[66]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[67]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  Robert T. Knight,et al.  Prefrontal cortex gating of auditory transmission in humans , 1989, Brain Research.

[69]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[70]  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.

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

[72]  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.

[73]  Joshua W. Brown,et al.  Monitoring and Control of Action by the Frontal Lobes , 2002, Neuron.

[74]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

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

[76]  C. D. Frith,et al.  Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations , 1995, The Lancet.

[77]  J. Fuster.  The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[78]  D. Pandya,et al.  Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey , 1988, The Journal of comparative neurology.

[79]  T. Braver,et al.  Anterior Cingulate Cortex and Response Conflict : Effects of Response Modality and Processing Domain , 2022 .

[80]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[81]  C Blakemore,et al.  Modulation of EPSP shape and efficacy by intrinsic membrane conductances in rat neocortical pyramidal neurons in vitro. , 1993, The Journal of physiology.

[82]  J. Sangiovanni,et al.  Increased GABAA receptor binding in superficial layers of cingulate cortex in schizophrenics , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  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.

[84]  Jonathan D. Cohen,et al.  Anterior cingulate and prefrontal cortex: who's in control? , 2000, Nature Neuroscience.

[85]  I. Divac.  Cortical circuits: Synaptic organization of the cerebral cortex. Structure, function and theory by Edward L. White, Birkäuser, 1989. Sw. fr. 88.00 (xvi + 223 pages) ISBN 3 7643 3402 9 , 1990, Trends in Neurosciences.

[86]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  Brent A. Vogt,et al.  Structure and Connections of the Cingulate Vocalization Region in the Rhesus Monkey , 1988 .

[88]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

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

[90]  A. Peters,et al.  The forms of non‐pyramidal neurons in the visual cortex of the rat , 1978, The Journal of comparative neurology.

[91]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets , 1994, The Journal of comparative neurology.

[92]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

[93]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[94]  T. Carr,et al.  Inhibitory Processes in Attention, Memory and Language , 1994 .

[95]  P. Goldman-Rakic,et al.  Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[96]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[97]  M. Posner,et al.  Executive attention: Conflict, target detection, and cognitive control. , 1998 .

[98]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

[99]  J. Newman.  The Physiological Control of Mammalian Vocalization , 1988, Springer US.

[100]  Yasuo Kawaguchi,et al.  Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. , 2006, Cerebral cortex.

[101]  Andrew J Trevelyan,et al.  Does inhibition balance excitation in neocortex? , 2005, Progress in biophysics and molecular biology.

[102]  C Frith,et al.  Brain mechanisms associated with top-down processes in perception. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[103]  Gang Tong,et al.  Multivesicular release from excitatory synapses of cultured hippocampal neurons , 1994, Neuron.

[104]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[105]  D L Woods,et al.  Electrophysiologic evidence of increased distractibility after dorsolateral prefrontal lesions , 1986, Neurology.

[106]  F. Benes,et al.  Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. , 1991, Archives of general psychiatry.

[107]  A. Larkman.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: I. Branching patterns , 1991, The Journal of comparative neurology.

[108]  J. Fiala,et al.  Computer-Based Alignment and Reconstruction of Serial Sections , 2006 .

[109]  Helen Barbas,et al.  Synaptic distinction of laminar-specific prefrontal-temporal pathways in primates. , 2006, Cerebral cortex.

[110]  P. Morgane,et al.  Comparative analysis of calcium-binding protein-immunoreactive neuronal populations in the auditory and visual systems of the bottlenose dolphin (Tursiops truncatus) and the macaque monkey (Macaca fascicularis) , 1998, Journal of Chemical Neuroanatomy.

[111]  R. Giberson,et al.  Microwave-Assisted Formalin Fixation of Fresh Tissue , 2001 .

[112]  F. Benes,et al.  Up-regulation of GABAA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects , 1996, Neuroscience.

[113]  V. Tennyson.  The Fine Structure of the Nervous System. , 1970 .

[114]  H. Barbas,et al.  Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey , 2005, BMC Neuroscience.

[115]  A. Arnsten,et al.  Neurobiology of Executive Functions: Catecholamine Influences on Prefrontal Cortical Functions , 2004, Biological Psychiatry.

[116]  P. Mu¨ller-Preuss,et al.  Inhibition of auditory cortical neurons during phonation , 1981, Brain Research.

[117]  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.

[118]  Andreas Burkhalter,et al.  Distinct GABAergic Targets of Feedforward and Feedback Connections Between Lower and Higher Areas of Rat Visual Cortex , 2003, The Journal of Neuroscience.

[119]  S. Palay,et al.  The Fine Structure of the Nervous System: Neurons and Their Supporting Cells , 1991 .

[120]  Christopher G. Wilson,et al.  A GABAergic inhibitory microcircuit controlling cholinergic outflow to the airways. , 2004, Journal of applied physiology.

[121]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.