GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus

The inferior colliculus (IC) is an important auditory processing center receiving inputs from lower brainstem nuclei, higher auditory and nonauditory structures, and contralateral IC. The IC, along with other auditory structures, is involved in coding information about the envelope of complex signals. Biologically relevant acoustic signals, including animal vocalizations and speech, are spectrally and temporally complex and display amplitude and frequency variations over time. Certain IC neurons respond selectively over a narrow range of modulation frequencies to sinusoidally amplitude modulated (SAM) stimuli. Responses to SAM stimuli can be measured in terms of discharge rate, with rate plotted against the modulation frequency to generate rate modulation transfer functions (rMTF). A role for the inhibitory neurotransmitter, gamma-aminobutyric acid (GABA), in shaping selective responses to SAM stimuli has been suggested. The present study examined the role of GABA in shaping responses to SAM stimuli in the IC of anesthetized chinchilla. Responses from 94 IC neurons were obtained before, during and after iontophoretic application of the GABA(A) receptor antagonist bicuculline methiodide. Complete responses to SAM stimuli were obtained from 55 extensively tested neurons, displaying band-pass (38) and low-pass rMTFs (17). For neurons showing band-pass rMTFs, GABA(A) receptor blockade selectively increased discharge rate at low modulation frequencies for 14 units, increased discharge near the best modulation frequency for 12 units. For neurons showing low-pass rMTFs, GABA(A) receptor blockade selectively increased discharge rate at low modulation frequencies for nine units. GABA(A) receptor blockade consistently reduced peak modulation gain, producing low-pass gain functions in a subset of IC neurons. In support of previous findings suggesting that selective temporal responses to SAM stimuli are coded in lower brainstem nuclei, temporal responses to SAM stimuli were relatively unaffected by GABA(A) receptor blockade. These findings support a role for GABA in shaping selective rate responses to SAM stimuli for a subset of chinchilla IC neurons.

[1]  J. H. Casseday,et al.  The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  D. Caspary,et al.  Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. , 1994, Journal of neurophysiology.

[3]  K. Osen,et al.  Anatomy of the inferior colliculus in rat , 2004, Anatomy and Embryology.

[4]  N. Akaike,et al.  Differential blockade of bicuculline and strychnine on GABA- and glycine-induced responses in dissociated rat hippocampal pyramidal cells , 1991, Brain Research.

[5]  A R Palmer,et al.  Rate-intensity functions and their modification by broadband noise for neurons in the guinea pig inferior colliculus. , 1988, The Journal of the Acoustical Society of America.

[6]  D. Caspary,et al.  Baclofen reduces tone-evoked activity of cochlear nucleus neurons , 1984, Hearing Research.

[7]  D. Caspary,et al.  Paired tone facilitation in dorsal cochlear nucleus neurons: A short-term potentiation model testable in vivo , 1994, Hearing Research.

[8]  D. Caspary,et al.  γ-Aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus , 1999, Hearing Research.

[9]  M. Semple,et al.  Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. , 2000, Journal of neurophysiology.

[10]  A S Feng,et al.  Oscillation May Play a Role in Time Domain Central Auditory Processing , 2001, The Journal of Neuroscience.

[11]  Y. Okada,et al.  Effect of GABA (γ-aminobutyric acid) on neurotransmission in inferior colliculus slices from the guinea pig , 1989, Neuroscience Research.

[12]  David R. Moore,et al.  Commissural and lemniscal synaptic input to the gerbil inferior colliculus. , 1998, Journal of neurophysiology.

[13]  G. C. Thompson,et al.  Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs , 1985, Brain Research.

[14]  R. Fay,et al.  The Mammalian auditory pathway : neurophysiology , 1992 .

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

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

[17]  D. Caspary,et al.  Responses of young and aged rat inferior colliculus neurons to sinusoidally amplitude modulated stimuli , 2001, Hearing Research.

[18]  R. Helfert,et al.  GABA and glycine immunoreactivity in the guinea pig superior olivary complex , 1989, Brain Research.

[19]  R. Roberts,et al.  GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil , 1987, The Journal of comparative neurology.

[20]  Katrin Reimer,et al.  Coding of sinusoidally amplitude modulated acoustic stimuli in the inferior colliculus of the rufous horseshoe bat,Rhinolophus rouxi , 1987, Journal of Comparative Physiology A.

[21]  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.

[22]  D. Caspary,et al.  Strychnine alters the fusiform cell output from the dorsal cochlear nucleus , 1987, Brain Research.

[23]  L. Li,et al.  Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  A. Nistri,et al.  Potentiating action of midazolam on GABA-mediated responses and its antagonism by Ro 14-7437 in the frog spinal cord , 1983, Neuroscience Letters.

[25]  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.

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

[27]  R. Batra,et al.  Temporal coding of envelopes and their interaural delays in the inferior colliculus of the unanesthetized rabbit. , 1989, Journal of neurophysiology.

[28]  T. Watanabe,et al.  Pharmacological properties of cat's collicular auditory neurons. , 1973, The Japanese journal of physiology.

[29]  J. Rockwood,et al.  Evidence for a GABAergic Projection from the Dorsal Nucleus of the Lateral Lemniscus to the Inferior Colliculus , 1993, Journal of neurochemistry.

[30]  M. Merchán,et al.  Dorsal nucleus of the lateral lemniscus in the rat: Concentric organization and tonotopic projection to the inferior colliculus , 1994, The Journal of comparative neurology.

[31]  Adrian Rees,et al.  Stimulus properties influencing the responses of inferior colliculus neurons to amplitude-modulated sounds , 1987, Hearing Research.

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

[33]  Joseph P. Walton,et al.  Dorsal cochlear nucleus single neurons can enhance temporal processing capabilities in background noise , 2004, Experimental Brain Research.

[34]  Robert D Frisina,et al.  Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement , 1990, Hearing Research.

[35]  G D Pollak,et al.  GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  R. Frisina,et al.  Differential encoding of rapid changes in sound amplitude by second-order auditory neurons , 2004, Experimental Brain Research.

[37]  Jim C. Hall.  Central Processing of Communication Sounds in the Anuran Auditory System , 1994 .

[38]  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.

[39]  G. Pollak,et al.  GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. Tohyama,et al.  Localization of GABAA-receptor alpha 1 subunit mRNA-containing neurons in the lower brainstem of the rat. , 1990, Brain research. Molecular brain research.

[41]  J. Winer,et al.  Morphology of GABAergic neurons in the inferior colliculus of the cat , 1994, The Journal of comparative neurology.

[42]  A. Rees,et al.  Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. , 1989, The Journal of the Acoustical Society of America.

[43]  W. S. Rhode,et al.  Encoding of amplitude modulation in the cochlear nucleus of the cat. , 1994, Journal of neurophysiology.

[44]  L. Aitkin,et al.  The responses of neurons in subdivisions of the inferior colliculus of cats to tonal, noise and vocal stimuli , 2004, Experimental Brain Research.

[45]  Z M Fuzessery,et al.  Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. , 1996, Journal of neurophysiology.

[46]  A. Kaneko,et al.  Effects of glycine and GABA on isolated bipolar cells of the mouse retina. , 1990, The Journal of physiology.

[47]  K. Glendenning,et al.  Acoustic chiasm V: Inhibition and excitation in the ipsilateral and contralateral projections of LSO , 1992, The Journal of comparative neurology.

[48]  D. Caspary,et al.  On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: iontophoretic studies , 1989, Brain Research.

[49]  R. M. Burger,et al.  Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. , 1998, Journal of neurophysiology.

[50]  A. Møller,et al.  Coding of amplitude and frequency modulated sounds in the cochlear nucleus of the rat. , 1972, Acta physiologica Scandinavica.

[51]  I. Fujita,et al.  The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  C. Faingold,et al.  Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons , 1993, Hearing Research.

[53]  D. Oliver,et al.  Connections of the dorsal nucleus of the lateral lemniscus: An inhibitory parallel pathway in the ascending auditory system? , 1988, The Journal of comparative neurology.

[54]  M. Merchán,et al.  Intrinsic and commissural connections of the rat inferior colliculus , 1992, The Journal of comparative neurology.

[55]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. , 1988, Journal of neurophysiology.

[56]  D. Oliver,et al.  EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: A possible source of inhibitory inputs to the inferior colliculus , 1989, The Journal of comparative neurology.

[57]  R. Altschuler,et al.  Neurobiology of hearing : the central auditory system , 1991 .

[58]  B. Grothe,et al.  GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. , 1998, Journal of neurophysiology.

[59]  Joe C. Adams,et al.  Dorsal nucleus of the lateral lemniscus: A nucleus of GABAergic projection neurons , 1984, Brain Research Bulletin.

[60]  D. Irvine.  Physiology of the Auditory Brainstem , 1992 .