Local connection patterns of parvalbumin-positive inhibitory interneurons in rat primary auditory cortex

In the auditory cortex (AC), GABAergic neurons constitute approximately 15-25% of all neurons. GABAergic cells are present in all sensory modalities and essential for modulating sensory receptive fields. Parvalbumin (PV) positive cells represent the largest sub-group of the GABAergic population in auditory neocortex. We investigated the projection pattern of PV cells in rat primary auditory cortex (AI) with a retrograde tracer (wheat germ apo-HRP conjugated to gold [WAHG]) and immunocytochemistry for PV. All AC layers except layer I contained cells double-labeled for PV and WAHG. All co-localized PV+ cells were within 2 mm of the injection site, regardless of laminar origin. Most (ca. 90%) of the co-localized PV cells were within 500 μm of the injection site in both dorsal-ventral and rostral-caudal dimension of the auditory core region. WAHG-only cells declined less rapidly with distance and were found up to 6 mm from the deposit sites. WAHG-only labeled cells in the medial geniculate body were in ventral division loci compatible with an injection in AI. Differences in the range and direction of the distribution pattern of co-localized PV+ cells and WAHG-only cells in AI express distinct functional convergence patterns for the two cell populations.

[1]  S. Hendry,et al.  GABA neuronal subpopulations in cat primary auditory cortex: co-localization with calcium binding proteins , 1991, Brain Research.

[2]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[3]  Henry Markram,et al.  Interneuron Diversity series: Molecular and genetic tools to study GABAergic interneuron diversity and function , 2004, Trends in Neurosciences.

[4]  A. Cowey,et al.  Retrograde transport of gamma-amino[3H]butyric acid reveals specific interlaminar connections in the striate cortex of monkey. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[5]  T. Kosaka,et al.  Cellular architecture of the mouse hippocampus: A quantitative aspect of chemically defined GABAergic neurons with stereology , 2006, Neuroscience Research.

[6]  MBA Enrico Bastianelli MD,et al.  Distribution of calcium-binding proteins in the cerebellum , 2003, The Cerebellum.

[7]  A. Schleicher,et al.  The ontogenetic development of serotonin (5-HT1) receptors in various cortical regions of the rat brain , 2004, Anatomy and Embryology.

[8]  E. G. Jones,et al.  Viewpoint: the core and matrix of thalamic organization , 1998, Neuroscience.

[9]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[10]  R A Reale,et al.  Geometry and orientation of neuronal processes in cat primary auditory cortex (AI) related to characteristic-frequency maps. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. D. de Venecia,et al.  A quantitative analysis of parvalbumin neurons in rabbit auditory neocortex , 1994, The Journal of comparative neurology.

[12]  C. Schreiner,et al.  A synaptic memory trace for cortical receptive field plasticity , 2007, Nature.

[13]  Enrico Bastianelli,et al.  Distribution of calcium-binding proteins in the cerebellum , 2008, The Cerebellum.

[14]  Christoph E. Schreiner,et al.  Functional topography of cat primary auditory cortex: representation of tone intensity , 2004, Experimental Brain Research.

[15]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[16]  S. Schiffmann,et al.  ‘New’ functions for ‘old’ proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice , 2002, The Cerebellum.

[17]  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.

[18]  J. Winer,et al.  Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

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

[20]  D P Phillips,et al.  Factors shaping the tone level sensitivity of single neurons in posterior field of cat auditory cortex. , 1995, Journal of neurophysiology.

[21]  E. G. Jones,et al.  Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Christoph E Schreiner,et al.  Spectrotemporal Processing Differences between Auditory Cortical Fast-Spiking and Regular-Spiking Neurons , 2008, The Journal of Neuroscience.

[23]  I. Ferrer,et al.  The development of parvalbumin-immunoreactivity in the neocortex of the mouse. , 1994, Brain research. Developmental brain research.

[24]  N. Tamamaki,et al.  Long‐range GABAergic projection neurons in the cat neocortex , 2007, The Journal of comparative neurology.

[25]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  H. Read,et al.  Multiparametric auditory receptive field organization across five cortical fields in the albino rat. , 2007, Journal of neurophysiology.

[27]  F. Fujiyama,et al.  Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex , 2005, The European journal of neuroscience.

[28]  J. Matsubara,et al.  Local, horizontal connections within area 18 of the cat. , 1988, Progress in brain research.

[29]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[30]  D. D. Greenwood,et al.  Excitatory and inhibitory response areas of auditory neurons in the cochlear nucleus. , 1965, Journal of neurophysiology.

[31]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[32]  A I Basbaum,et al.  Wheat germ agglutinin‐apoHRP gold: A new retrograde tracer for light‐ and electron‐microscopic single‐ and double‐label studies , 1987, The Journal of comparative neurology.

[33]  A. Cowey,et al.  Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey , 1981, Nature.

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

[35]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[36]  K. Albus,et al.  The Topography of Tangential Inhibitory Connections in the Postnatally Developing and Mature Striate Cortex of the Cat , 1994, The European journal of neuroscience.

[37]  T. Kaneko,et al.  Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse , 2003, The Journal of comparative neurology.

[38]  Guangying K. Wu,et al.  Nonmonotonic Synaptic Excitation and Imbalanced Inhibition Underlying Cortical Intensity Tuning , 2006, Neuron.

[39]  M. Fabri,et al.  Glutamate decar☐ylase immunoreactivity in corticocortical projecting neurons of rat somatic sensory cortex , 1996, Neuroscience.

[40]  J. Boyd,et al.  Presence of GABA-immunoreactive neurons within intracortical patches in area 18 of the cat , 1992, Brain Research.

[41]  Guangying K. Wu,et al.  Lateral Sharpening of Cortical Frequency Tuning by Approximately Balanced Inhibition , 2008, Neuron.

[42]  A. Basbaum A rapid and simple silver enhancement procedure for ultrastructural localization of the retrograde tracer WGAapoHRP-Au and its use in double-label studies with post-embedding immunocytochemistry. , 1989, Journal of Histochemistry and Cytochemistry.

[43]  J. Winer,et al.  Origins of medial geniculate body projections to physiologically defined zones of rat primary auditory cortex , 1999, Hearing Research.

[44]  Stéphane Charpier,et al.  Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo , 2005, The Journal of Neuroscience.

[45]  M. M. Merzenich,et al.  Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons , 2006, Neuroscience.

[46]  C. Schreiner,et al.  Modular organization of frequency integration in primary auditory cortex. , 2000, Annual review of neuroscience.

[47]  K. Albus,et al.  The contribution of GABA-ergic neurons to horizontal intrinsic connections in upper layers of the cat's striate cortex , 2004, Experimental Brain Research.