Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat

The inferior colliculus (IC) is a major auditory structure that integrates synaptic inputs from ascending, descending, and intrinsic sources. Intracellular recording in situ allows direct examination of synaptic inputs to the IC in response to acoustic stimulation. Using this technique and monaural or binaural stimulation, responses in the IC that reflect input from a lower center can be distinguished from responses that reflect synaptic integration within the IC. Our results indicate that many IC neurons receive synaptic inputs from multiple sources. Few, if any, IC neurons acted as simple relay cells. Responses often displayed complex interactions between excitatory and inhibitory sources, such that different synaptic mechanisms could underlie similar response patterns. Thus, it may be an oversimplification to classify the responses of IC neurons as simply excitatory or inhibitory, as is done in many studies. In addition, inhibition and intrinsic membrane properties appeared to play key roles in creating de novo temporal response patterns in the IC.

[1]  S Kuwada,et al.  Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: effects of sodium pentobarbital. , 1989, Journal of neurophysiology.

[2]  L. Carney,et al.  Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: excitatory and inhibitory components. , 1989, Journal of neurophysiology.

[3]  R. Batra,et al.  Interaural phase-sensitive units in the inferior colliculus of the unanesthetized rabbit: effects of changing frequency. , 1987, Journal of neurophysiology.

[4]  E G Jones,et al.  The neuronal organization of the inferior colliculus of the adult cat. I. The central nucleus , 1973, The Journal of comparative neurology.

[5]  T. Yin,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. , 1983, Journal of neurophysiology.

[6]  D. Anderson,et al.  Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. , 1970, Journal of neurophysiology.

[7]  R. Andersen,et al.  The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat , 1980, The Journal of comparative neurology.

[8]  T. Powell,et al.  The projection of the auditory cortex upon the diencephalon and brain stem in the cat. , 1969, Brain research.

[9]  J. E. Hind,et al.  Interaural time differences: implications regarding the neurophysiology of sound localization. , 1980, The Journal of the Acoustical Society of America.

[10]  D. Oertel,et al.  Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  S. Erulkar,et al.  SYNAPTIC MECHANISMS OF EXCITATION AND INHIBITION IN THE CENTRAL AUDITORY PATHWAY. , 1963, Journal of neurophysiology.

[12]  K. Glendenning,et al.  Acoustic chiasm: efferent projections of the lateral superior olive , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  D. Oliver,et al.  The central nucleus of the inferior colliculus in the cat , 1984, The Journal of comparative neurology.

[14]  S. Nomura,et al.  Effects of stimulation of the primary auditory cortex upon colliculogeniculate neurons in the inferior colliculus of the cat , 1983, Neuroscience Letters.

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

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

[17]  S Kuwada,et al.  A comparison of the interaural time sensitivity of neurons in the inferior colliculus and thalamus of the unanesthetized rabbit , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  E. Ağar,,et al.  Physiological-Morphologial Properties Of The Anteroventral Cochlear Nucleus , 1997 .

[19]  D. Irvine The Auditory Brainstem , 1986, Progress in Sensory Physiology.

[20]  S Kuwada,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. I. Effects of long interaural delays, intensity, and repetition rate on interaural delay function. , 1983, Journal of neurophysiology.

[21]  D C Fitzpatrick,et al.  Neural responses to simple simulated echoes in the auditory brain stem of the unanesthetized rabbit. , 1995, Journal of neurophysiology.

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

[23]  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.

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

[25]  W. R. Webster,et al.  Discharge patterns of single units in inferior colliculus of the alert cat. , 1972, Journal of neurophysiology.

[26]  R. Batra,et al.  A physiological and structural study of neuron types in the cochlear nucleus. I. Intracellular responses to acoustic stimulation and current injection , 1994, The Journal of comparative neurology.

[27]  D O Kim,et al.  Responses of auditory nerve fibers of the unanesthetized decerebrate cat to click pairs as simulated echoes. , 1996, Journal of neurophysiology.

[28]  M. Conley,et al.  The distribution of glutamic acid decarboxylase immunoreactivity in the diencephalon of the opossum and rabbit , 1984, The Journal of comparative neurology.

[29]  T. Yin,et al.  Dendritic and axonal morphology of HRP‐injected neurons in the inferior colliculus of the cat , 1991, The Journal of comparative neurology.

[30]  S Kuwada,et al.  Response of cat inferior colliculus neurons to binaural beat stimuli: possible mechanisms for sound localization. , 1979, Science.

[31]  T. Yin,et al.  Interaural time sensitivity in medial superior olive of cat. , 1990, Journal of neurophysiology.

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

[33]  D. Oliver,et al.  Ascending Projections from the Cochlear Nucleus to the Inferior Colliculus and their Interactions with Projections from the Superior Olivary Complex , 1993 .

[34]  K. A. Fitzpatrick Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey , 1975, The Journal of comparative neurology.

[35]  J. Kelly,et al.  Effects of superior olivary comples lesions on binaural responses in rat inferior colliculus , 1992, Brain Research.

[36]  R. L. Marie,et al.  Glycine‐immunoreactive projection of the cat lateral superior olive: Possible role in midbrain ear dominance , 1989, The Journal of comparative neurology.

[37]  PB Manis,et al.  Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  D. Oliver,et al.  The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain , 1984, The Journal of comparative neurology.

[39]  C. K. Henkel,et al.  Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods , 1983, The Journal of comparative neurology.

[40]  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.

[41]  R. Batra,et al.  High-frequency neurons in the inferior colliculus that are sensitive to interaural delays of amplitude-modulated tones: evidence for dual binaural influences. , 1993, Journal of neurophysiology.

[42]  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.

[43]  P. Torterolo,et al.  In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs , 1997, Brain Research.

[44]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[45]  E. Covey The Monaural Nuclei of the Lateral Lemniscus: Parallel Pathways from Cochlear Nucleus to Midbrain , 1993 .

[46]  A. Rockel,et al.  The neuronal organization of the inferior colliculus of the adult cat. II. The pericentral nucleus , 1973, The Journal of comparative neurology.

[47]  T. Yin,et al.  Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  J. Eccles,et al.  Electrophysiological investigations on Renshaw cells , 1961, The Journal of physiology.

[49]  T. Yin,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. , 1983, Journal of neurophysiology.

[50]  M. F. Huerta,et al.  Inferior and Superior Colliculi , 1992 .

[51]  J. Guinan,et al.  Single auditory units in the superior olivary complex , 1972 .

[52]  J. Guinan,et al.  Single Auditory Units in the Superior Olivary Complex: II: Locations of Unit Categories and Tonotopic Organization , 1972 .

[53]  J. Kauer,et al.  Whole-Cell Patch-Clamp Recording Reveals Subthreshold Sound-Evoked Postsynaptic Currents in the Inferior Colliculus of Awake Bats , 1996, The Journal of Neuroscience.

[54]  S Kuwada,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. IV. Comparison of monaural and binaural response properties. , 1984, Journal of neurophysiology.

[55]  M. C. Citron,et al.  The jet stream microbeveler: an inexpensive way to bevel ultrafine glass micropipettes. , 1978, Science.