Divergent response properties of layer-V neurons in rat primary auditory cortex

Layer-V pyramidal cells comprise a major output of primary auditory cortex (A1). At least two cell types displaying different morphology, projections and in vitro physiology have been previously identified in layer-V. The focus of the present study was to characterize extracellular receptive field properties of layer-V neurons to determine whether a similar breakdown of responses can be found in vivo. Recordings from 105 layer-V neurons revealed two predominant receptive field types. Thirty-two percent displayed strong excitatory V/U-shaped receptive field maps and spiking patterns with shorter stimulus-driven interspike intervals (ISIs), reminiscent of the bursting cells discussed in the in vitro literature. V/U-shaped maps remained relatively unchanged across the three sequential repetitions of the map run on each neuron. Neurons with V/U-shaped maps were also easily depolarized with extracellular current pulse stimulation. In contrast, 47% of the neurons displayed Complex receptive field maps characterized by weak and/or inconsistent excitatory regions and were difficult to depolarize with current pulses. These findings suggest that V/U-shaped receptive fields could correspond to previously described intrinsic bursting (IB) cells with corticotectal projections, and that neurons with Complex receptive fields might represent the regular spiking (RS) cells with their greater inhibitory input and corticocortical/corticostriatal projection pattern.

[1]  B. Connors,et al.  Laminar origins of inhibitory synaptic inputs to pyramidal neurons of the rat neocortex. , 1996, The Journal of physiology.

[2]  R. Reale,et al.  Auditory cortical field projections to the basal ganglia of the cat , 1983, Neuroscience.

[3]  P. Jen,et al.  Corticofugal inhibition compresses all types of rate-intensity functions of inferior collicular neurons in the big brown bat , 2000, Brain Research.

[4]  D. W. Vaughan,et al.  Thalamic and callosal connections of the rat auditory cortex , 1983, Brain Research.

[5]  O. W. Henson,et al.  The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus , 1990, Brain Research Reviews.

[6]  J. Winer,et al.  Columnar organization and reciprocity of commissural connections in cat primary auditory cortex (AI) , 1986, Hearing Research.

[7]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[8]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: sound frequency. , 1988, Journal of neurophysiology.

[9]  Nobuo Suga,et al.  Corticofugal modulation of the midbrain frequency map in the bat auditory system , 1998, Nature Neuroscience.

[10]  J. Coleman,et al.  Sources of projections to subdivisions of the inferior colliculus in the rat , 1987, The Journal of comparative neurology.

[11]  Joseph E LeDoux,et al.  Redefining the tonotopic core of rat auditory cortex: Physiological evidence for a posterior field , 2002, The Journal of comparative neurology.

[12]  N. Suga,et al.  Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  T. Hattori,et al.  Pyramidal cells in rat temporoauditory cortex project to both striatum and inferior colliculus , 1991, Brain Research Bulletin.

[14]  P. Jen,et al.  Brief and short-term corticofugal modulation of subcortical auditory responses in the big brown bat, Eptesicus fuscus. , 2000, Journal of neurophysiology.

[15]  D. Ryugo,et al.  The cellular origin of corticofugal projections to the superior olivary complex in the rat , 2002, Brain Research.

[16]  Koji Hara,et al.  Anesthetic Pharmacology International Society for Anaesthetic Pharmacology the Anesthetic Mechanism of Urethane: the Effects on Neurotransmitter-gated Ion Channels , 2022 .

[17]  B. Schofield,et al.  Projections from the auditory cortex to the superior olivary complex in guinea pigs , 2004, The European journal of neuroscience.

[18]  E. Mugnaini,et al.  Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections , 1996, The Journal of comparative neurology.

[19]  N Suga,et al.  Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. , 2000, Journal of neurophysiology.

[20]  G. Ehret,et al.  Corticofugal modulation of midbrain sound processing in the house mouse , 2002, The European journal of neuroscience.

[21]  P. Pilowsky,et al.  Juxtacellular labeling of identified neurons: Kiss the cells and make them dye , 2001, The Journal of comparative neurology.

[22]  M. Kilgard,et al.  Plasticity of temporal information processing in the primary auditory cortex , 1998, Nature Neuroscience.

[23]  D. Ryugo,et al.  Pyramidal cells in primary auditory cortex project to cochlear nucleus in rat , 1996, Brain Research.

[24]  Norman M. Weinberger,et al.  Physiological Memory in Primary Auditory Cortex: Characteristics and Mechanisms , 1998, Neurobiology of Learning and Memory.

[25]  Manfred Kössl,et al.  Laminar Analysis of Inhibition in the Gerbil Primary Auditory Cortex , 2001, Journal of the Association for Research in Otolaryngology.

[26]  B. Connors,et al.  Repetitive burst-firing neurons in the deep layers of mouse somatosensory cortex , 1989, Neuroscience Letters.

[27]  D. Caspary,et al.  GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. , 1996, Journal of neurophysiology.

[28]  Philip H Smith,et al.  Distribution and Kinetic Properties of GABAergic Inputs to Layer V Pyramidal Cells in Rat Auditory Cortex , 2003, Journal of the Association for Research in Otolaryngology.

[29]  P. Jen,et al.  Corticofugal influences on the responses of bat inferior collicular neurons to sound stimulation , 1989, Brain Research.

[30]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[31]  J. Winer,et al.  Corticocortical connections of cat primary auditory cortex (AI): Laminar organization and identification of supragranular neurons projecting to area AII , 1986, The Journal of comparative neurology.

[32]  J. Winer,et al.  Auditory cortical projections to the cat inferior colliculus , 1998, The Journal of comparative neurology.

[33]  N Suga,et al.  Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. , 1997, Journal of neurophysiology.

[34]  Jun Yan,et al.  Corticofugal reorganization of the midbrain tonotopic map in mice , 2001, Neuroreport.

[35]  H Scheich,et al.  Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections , 2000, The European journal of neuroscience.

[36]  S. A. Colwell Thalamocortical-corticothalamic reciprocity: a combined anterograde-retrograde tracer technique , 1975, Brain Research.

[37]  Philip H Smith,et al.  Anatomy, Physiology, and Synaptic Responses of Rat Layer V Auditory Cortical Cells and Effects of Intracellular GABAABlockade , 2000 .

[38]  A. Leventhal,et al.  GABA and Its Agonists Improved Visual Cortical Function in Senescent Monkeys , 2003, Science.

[39]  J. Winer The Functional Architecture of the Medial Geniculate Body and the Primary Auditory Cortex , 1992 .

[40]  N Suga,et al.  The corticofugal system for hearing: recent progress. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Winer,et al.  Layer V in cat primary auditory cortex (AI): Cellular architecture and identification of projection neurons , 2001, The Journal of comparative neurology.

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

[43]  J. Popelář,et al.  Inferior colliculus in the rat: Neuronal responses to stimulation of the auditory cortex , 1984, Neuroscience Letters.

[44]  E. G. Jones,et al.  Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. , 1992, Cerebral cortex.

[45]  E. Friauf,et al.  Commissural connections between the auditory cortices of the rat , 1990, Brain Research.

[46]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[47]  M. Deschenes,et al.  Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1994, Brain Research.

[48]  P. Torterolo,et al.  Auditory cortical efferent actions upon inferior colliculus unitary activity in the guinea pig , 1998, Neuroscience Letters.

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

[50]  Josef P. Rauschecker,et al.  Auditory cortical plasticity: a comparison with other sensory systems , 1999, Trends in Neurosciences.

[51]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

[52]  J. Winer,et al.  Auditory connections and neurochemistry of the sagulum , 1998, The Journal of comparative neurology.

[53]  H. Faye-Lund,et al.  The neocortical projection to the inferior colliculus in the albino rat , 2004, Anatomy and Embryology.

[54]  L. Aitkin,et al.  The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus , 1981, The Journal of comparative neurology.

[55]  H. Scheich,et al.  Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures , 2000, The European journal of neuroscience.

[56]  Jian Wang,et al.  Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons , 2002, Brain Research.

[57]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[58]  B. Connors,et al.  Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. , 1999, Journal of neurophysiology.

[59]  C. Maggi,et al.  Suitability of urethane anesthesia for physiopharmacological investigations in various systems Part 1: General considerations , 1986, Experientia.

[60]  D. Prince,et al.  Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features , 1990, The Journal of comparative neurology.

[61]  J. Winer,et al.  Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex , 1988, Hearing Research.

[62]  M. Sutter Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. , 2000, Journal of neurophysiology.

[63]  Joachim Ostwald,et al.  Topography of projections from the auditory cortex to the inferior colliculus in the rat , 1991, The Journal of comparative neurology.

[64]  D. Ryugo,et al.  Projections from auditory cortex to the cochlear nucleus in rats: Synapses on granule cell dendrites , 1996, The Journal of comparative neurology.