Spatial representation of corticofugal input in the inferior colliculus: a multicontact silicon probe approach

The inferior colliculus (IC) is a well-established target of descending projections from the auditory cortex (AC). However, our understanding of these pathways has been limited by an incomplete picture of their functional influence within the three-dimensional space of the IC. Our goal was to study the properties and spatial representation of corticofugal input in the IC of guinea pigs with a high degree of spatial resolution. We systematically mapped neural activity in the IC using two types of silicon substrate probes that allow for simultaneous recording at multiple neural sites. One probe provided a high resolution in the dorsal-ventral plane and the other provided spatial resolution in the medial-lateral plane. Electrical stimulation of the ipsilateral AC produced excitatory responses in the IC with thresholds usually below 5–10 µA. First spike latencies were predominantly in the 6–20 ms range, although latencies from 3–5 ms were also observed. Broadly distributed unimodal spike patterns with modal latencies greater than 30 ms were occasionally seen. The excitatory responses to cortical stimulation were mostly unimodal and occasionally bimodal with a wide range of spike distribution patterns and response durations. Excitation was often followed by suppression of spontaneous activity. Suppression of acoustic responses was observed even when there was little or no response to electrical stimulation, suggesting spatial-temporal integration. A few of the responding neurons showed purely inhibitory responses to electrical stimulation, suggesting that there are disynaptic routes of corticocollicular inhibition. Detailed spatial mapping revealed that the response patterns and their durations had a characteristic spatial distribution in the IC.

[1]  T. Imig,et al.  Projections of auditory cortex upon the thalamus and Midbrain in the owl monkey , 1978, The Journal of comparative neurology.

[2]  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.

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

[4]  M. A. Johnson,et al.  Chronic recording of regenerating VIIIth nerve axons with a sieve electrode. , 2000, Journal of neurophysiology.

[5]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  O D Creutzfeldt,et al.  Functional subdivisions in the auditory cortex of the guinea pig , 1989, The Journal of comparative neurology.

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

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

[9]  B. Beyerl.  Afferent projections to the central nucleus of the inferior colliculus in the rat , 1978, Brain Research.

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

[11]  L. Aitkin.  The Auditory Midbrain: Structure and Function in the Central Auditory Pathway , 1986 .

[12]  N. Suga,et al.  Corticofugal modulation of frequency processing in bat auditory system , 1997, Nature.

[13]  G. Rajkowska,et al.  Projections of auditory cortex onto the inferior colliculus in the rat. , 1997, Physiological research.

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

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

[16]  A Kral,et al.  Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. , 1999, Science.

[17]  N. Suga,et al.  Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[19]  The Auditory Midbrain: Structure and Function in the Central Auditory Pathway. , 1986 .

[20]  J. Popelář,et al.  Descending Central Auditory Pathway — Structure and Function , 1988 .

[21]  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.

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

[23]  Josef Syka,et al.  Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. , 2002, Physiological reviews.

[24]  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.

[25]  R. Altschuler,et al.  Deafness-induced plasticity in the mature central auditory system , 1995, Neuroreport.

[26]  P. Jen,et al.  Corticofugal regulation of auditory sensitivity in the bat inferior colliculus , 1998, Journal of Comparative Physiology A.

[27]  N Suga,et al.  Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  G. Langner,et al.  Computer simulation of a tinnitus model based on labelling of tinnitus activity in the auditory cortex. J. Hazel , 1999 .

[29]  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.

[30]  J. Kelly,et al.  Laminar connections of the cat's auditory cortex , 1981, Brain Research.

[31]  J. Chen.  A Multichannel Neural Probe for Selective Chemical Delivery at the Cellular Level , 1997 .

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

[33]  R. Klinke,et al.  Hearing after congenital deafness: central auditory plasticity and sensory deprivation. , 2002, Cerebral cortex.

[34]  N. Suga,et al.  Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  N. Suga,et al.  Plasticity of bat's central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. , 2001, Journal of neurophysiology.

[36]  K. Wise,et al.  A high-yield IC-compatible multichannel recording array , 1985, IEEE Transactions on Electron Devices.

[37]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[38]  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.

[39]  J. Syka,et al.  Ascending and descending projections to the inferior colliculus in the rat. , 1984, Physiologia Bohemoslovaca.

[40]  N Suga,et al.  Corticofugal Modulation of Time-Domain Processing of Biosonar Information in Bats , 1996, Science.

[41]  N. Suga,et al.  Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. , 1999, Journal of neurophysiology.

[42]  T. Elbert,et al.  Reorganization of auditory cortex in tinnitus. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  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.

[44]  The auditory midbrain , 1979, Trends in Neurosciences.

[45]  K. Wise,et al.  A three-dimensional microelectrode array for chronic neural recording , 1994, IEEE Transactions on Biomedical Engineering.

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

[47]  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.

[48]  S. Potashner,et al.  Evidence for a Glutamatergic Pathway from the Guinea Pig Auditory Cortex to the Inferior Colliculus , 1995, Journal of neurochemistry.

[49]  K. Wise,et al.  An implantable CMOS circuit interface for multiplexed microelectrode recording arrays , 1992 .

[50]  G. C. Thompson,et al.  HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat , 1981, The Journal of comparative neurology.

[51]  J. Winer,et al.  Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey , 2002, Hearing Research.

[52]  C. Wilson,et al.  Multiple site silicon-based probes for chronic recordings in freely moving rats: implantation, recording and histological verification , 2000, Journal of Neuroscience Methods.

[53]  I. T. Diamond,et al.  The function of the tectum for attention to auditory stimuli in the cat , 1965, The Journal of comparative neurology.