Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons

Neurons containing gamma aminobutyric acid (GABA) are widely distributed throughout the primary auditory cortex (AI). We investigated the effects of endogenous GABA by comparing response properties of 110 neurons in chinchilla AI before and after iontophoresis of bicuculline, a GABA(A) receptor antagonist, and/or CGP35348, a GABA(B) receptor antagonist. GABA(A) receptor blockade significantly increased spontaneous and driven discharge rates, dramatically decreased the thresholds of many neurons, and constricted the range of thresholds across the neural population. Some neurons with 'non-onset' temporal discharge patterns developed an onset pattern that was followed by a long pause. Interestingly, the excitatory response area typically expanded on both sides of the characteristic frequency; this expansion exceeded one octave in a third of the sample. Although GABA(B) receptor blockade had little effect alone, the combination of CGP35348 and bicuculline produced greater increases in driven rate and expansion of the frequency response area than GABA(A) receptor blockade alone, suggesting a modulatory role of local GABA(B) receptors. The results suggest that local GABA inhibition contributes significantly to intensity and frequency coding by controlling the range of intensities over which cortical neurons operate and the range of frequencies to which they respond. The inhibitory circuits that generate nonmonotonic rate-level functions are separate from those that influence other response properties of AI neurons.

[1]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[2]  R. Knight,et al.  Auditory evoked potentials from the primary auditory cortex of the cat: topographic and pharmacological studies. , 1990, Electroencephalography and clinical neurophysiology.

[3]  L. Aitkin,et al.  Medial geniculate body: unit responses in the awake cat. , 1974, Journal of neurophysiology.

[4]  N. Weinberger,et al.  Muscarinic agonists modulate spontaneous and evoked unit discharge in auditory cortex of cat , 1988, Synapse.

[5]  G D Pollak,et al.  GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. , 1992, Journal of neurophysiology.

[6]  L. Aitkin,et al.  Plasticity of auditory cortex associated with sensorineural hearing loss in adult C57BL/6J mice , 1993, The Journal of comparative neurology.

[7]  J. Winer,et al.  Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

[8]  N. Bowery,et al.  Inhibition of GABAB Receptor Binding by Guanyl Nucleotides , 1984, Journal of neurochemistry.

[9]  D. Irvine,et al.  Neuronal Responses across Cortical Field A1 in Plasticity Induced by Peripheral Auditory Organ Damage , 1998, Audiology and Neurotology.

[10]  D. R. Curtis,et al.  GABA, Bicuculline and Central Inhibition , 1970, Nature.

[11]  J. C. Hall GABAergic inhibition shapes frequency tuning and modifies response properties in the auditory midbrain of the leopard frog , 1999, Journal of Comparative Physiology A.

[12]  J. Winer Neurons accumulating [3Hgamma-aminobutyric acid (GABA) in supragranular layers of cat primary auditory cortex (AI) , 1986, Neuroscience.

[13]  R. Rajan,et al.  Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. , 2001, Cerebral cortex.

[14]  M. Merzenich,et al.  Neuronal discharge rate is unsuitable for encoding sound intensity at the inferior-colliculus level , 1988, Hearing Research.

[15]  M. Merzenich,et al.  Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. , 1973, Journal of neurophysiology.

[16]  Björn Capsius,et al.  Influence of urethane anesthesia on neural processing in the auditory cortex analogue of a songbird , 1996, Hearing Research.

[17]  J. Willott,et al.  Paleocerebellar lesions enhance audiogenic seizures in mice , 1978, Experimental Neurology.

[18]  Ramesh Rajan,et al.  Injury- and Use-Related Plasticity in Adult Auditory Cortex , 2001, Audiology and Neurotology.

[19]  D. P. Phillips,et al.  Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity differences , 1981, Hearing Research.

[20]  R. Metherate,et al.  Synaptic interactions involving acetylcholine, glutamate, and GABA in rat auditory cortex , 2004, Experimental Brain Research.

[21]  G. Orban,et al.  Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex , 1995, The Journal of comparative neurology.

[22]  D. Caspary,et al.  A simple technique for constructing 'piggy-back' multibarrel microelectrodes. , 1980, Electroencephalography and clinical neurophysiology.

[23]  D. P. Phillips,et al.  Some neural mechanisms in the cat's auditory cortex underlying sensitivity to combined tone and wide-spectrum noise stimuli , 1985, Hearing Research.

[24]  C. Tanaka,et al.  Benzodiazepines and barbiturate potentiate the pre- and postsynaptic gamma-aminobutyric acid (GABA)A receptor-mediated response in the enteric nervous system of guinea pig small intestine. , 1988, The Journal of pharmacology and experimental therapeutics.

[25]  G. Pollak,et al.  The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus , 1993, Hearing Research.

[26]  U. Misgeld,et al.  A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system , 1995, Progress in Neurobiology.

[27]  N. Bowery,et al.  3H-baclofen and 3H-GABA bind to bicuculline-insensitive GABAB sites in rat brain , 1981, Nature.

[28]  E. G. Jones,et al.  Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17 , 1986, Nature.

[29]  M. Schmutz,et al.  GABAB receptors in various in vitro and in vivo models of epilepsy: A study with the GABAB receptor blocker CGP 35348 , 1992, Neuroscience.

[30]  B. Grothe,et al.  The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats , 2004, Journal of Comparative Physiology A.

[31]  R. Helfert,et al.  Central auditory aging: GABA changes in the inferior colliculus , 1995, Experimental Gerontology.

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

[33]  Norman M. Weinberger,et al.  Synaptic potentials and effects of amino acid antagonists in the auditory cortex , 1992, Brain Research Bulletin.

[34]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[35]  J. Edeline,et al.  Effects of noradrenaline on rate-level function of auditory cortex neurons: Is there a “gating” effect of noradrenaline? , 1998, Experimental Brain Research.

[36]  K. A. Davis,et al.  Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. , 1999, Journal of neurophysiology.

[37]  D. C. Teas,et al.  Single unit study of binaural interaction in the auditory cortex of the chinchilla , 1976, Brain Research.

[38]  J. Disterhoft,et al.  Location of rabbit auditory cortex and description of single unit activity , 1981, Brain Research.

[39]  B. Bettler,et al.  Expression cloning of GABAB receptors uncovers similarity to metabotropic glutamate receptors , 1997, Nature.

[40]  M Abeles,et al.  Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs. , 1972, Brain research.

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

[42]  M. Krasowski,et al.  Intravenous Anesthetics Differentially Modulate Ligand-gated Ion Channels , 2000, Anesthesiology.

[43]  N. Kiang,et al.  LIV A Survey of Recent Developments in the Study of Auditory Physiology , 1968, The Annals of otology, rhinology, and laryngology.

[44]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

[45]  D P Phillips,et al.  Responses of single neurons in posterior field of cat auditory cortex to tonal stimulation. , 1984, Journal of neurophysiology.

[46]  M M Merzenich,et al.  Auditory midbrain responses parallel spectral integration phenomena. , 1985, Science.

[47]  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.

[48]  N. Harel,et al.  Tonotopic mapping in auditory cortex of the chinchilla , 1996, Hearing Research.

[49]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[50]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[51]  Donald Robertson,et al.  Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness , 1989, The Journal of comparative neurology.

[52]  M. Kubota,et al.  Optical imaging of spatiotemporal patterns of glutamatergic excitation and GABAergic inhibition in the guinea‐pig auditory cortex in vivo. , 1996, The Journal of physiology.

[53]  D. Caspary,et al.  Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons , 1991, Hearing Research.

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

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

[56]  N. Neff,et al.  gamma-aminobutyric acid B receptors are negatively coupled to adenylate cyclase in brain, and in the cerebellum these receptors may be associated with granule cells. , 1984, Molecular pharmacology.

[57]  G. Fagg,et al.  CGP 35348: a centrally active blocker of GABAB receptors. , 1990, European journal of pharmacology.

[58]  J. Winer,et al.  Auditory thalamocortical projections in the cat: Laminar and areal patterns of input , 2000, The Journal of comparative neurology.

[59]  R. Metherate,et al.  GABAergic suppression prevents the appearance and subsequent fatigue of an NMDA receptor-mediated potential in neocortex , 1995, Brain Research.

[60]  J. Roder,et al.  Blockade of glutamate receptors and barbiturate anesthesia: increased sensitivity to pentobarbital-induced anesthesia despite reduced inhibition of AMPA receptors in GluR2 null mutant mice. , 1999, Anesthesiology.

[61]  P. Land,et al.  Activity‐dependent regulation of glutamic acid decarboxylase in the rat barrel cortex: Effects of neonatal versus adult sensory deprivation , 1991, The Journal of comparative neurology.

[62]  S. Brandner,et al.  The projection from medial geniculate to field AI in cat: organization in the isofrequency dimension , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Edeline,et al.  Effects of Noradrenaline on Frequency Tuning of Rat Auditory Cortex Neurons , 1997, The European journal of neuroscience.

[64]  D. R. Curtis,et al.  Bicuculline and Central GABA Receptors , 1970, Nature.

[65]  D. Caspary,et al.  Effects of microiontophoretically applied glycine and GABA on neuronal response patterns in the cochlear nuclei , 1979, Brain Research.

[66]  M. Liberman,et al.  Auditory-nerve response from cats raised in a low-noise chamber. , 1978, The Journal of the Acoustical Society of America.

[67]  F. de Ribaupierre,et al.  Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions , 1994, Neuroscience Research.

[68]  D. Irvine,et al.  Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex , 1993, The Journal of comparative neurology.

[69]  K. Niimi,et al.  Cortical projections of the medial geniculate body in the cat , 1974, Experimental Brain Research.

[70]  S. Enna,et al.  Biochemical and electrophysiological characteristics of mammalian GABA receptors. , 1983, International review of neurobiology.

[71]  M S Malmierca,et al.  Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. , 1996, Journal of neurophysiology.

[72]  Drf Irvine,et al.  INJURY‐ AND USE‐RELATED PLASTICITY IN THE PRIMARY SENSORY CORTEX OF ADULT MAMMALS: POSSIBLE RELATIONSHIP TO PERCEPTUAL LEARNING , 1996, Clinical and experimental pharmacology & physiology.

[73]  J. Winer Identification and structure of neurons in the medial geniculate body projecting to primary auditory cortex (AI) in the cat , 1984, Neuroscience.