Responses in the inferior colliculus of the guinea pig to concurrent harmonic series and the effect of inactivation of descending controls.

One of the fundamental questions of auditory research is how sounds are segregated because, in natural environments, multiple sounds tend to occur at the same time. Concurrent sounds, such as two talkers, physically add together and arrive at the ear as a single input sound wave. The auditory system easily segregates this input into a coherent perception of each of the multiple sources. A common feature of speech and communication calls is their harmonic structure and in this report we used two harmonic complexes to study the role of the corticofugal pathway in the processing of concurrent sounds. We demonstrate that, in the inferior colliculus (IC) of the anesthetized guinea pig, deactivation of the auditory cortex altered the temporal and/or the spike response to the concurrent, monaural harmonic complexes. More specifically, deactivating the auditory cortex altered the representation of the relative level of the complexes. This suggests that the auditory cortex modulates the representation of the level of two harmonic complexes in the IC. Since sound level is a cue used in the segregation of auditory input, the corticofugal pathway may play a role in this segregation.

[1]  A. Rees,et al.  Compact and easy-to-use tungsten-in-glass microelectrode manufacturing workstation , 1988, Medical and Biological Engineering and Computing.

[2]  W. S. Rhode,et al.  Responses of fibers in the cat's auditory nerve to the cubic difference tone. , 1978, The Journal of the Acoustical Society of America.

[3]  J. Kelly,et al.  Glutamatergic and GABAergic regulation of neural responses in inferior colliculus to amplitude-modulated sounds. , 2003, Journal of neurophysiology.

[4]  G. Biggio,et al.  Actions of the general anesthetic propofol on recombinant human GABAA receptors: influence of receptor subunits. , 1995, The Journal of pharmacology and experimental therapeutics.

[5]  L R Soma,et al.  ANESTHETIC AND ANALGESIC CONSIDERATIONS IN THE EXPERIMENTAL ANIMAL , 1983, Annals of the New York Academy of Sciences.

[6]  E. Kvašňák,et al.  Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. , 1996, Audiology : official organ of the International Society of Audiology.

[7]  B. Delgutte,et al.  Pitch representations in the auditory nerve: two concurrent complex tones. , 2008, Journal of neurophysiology.

[8]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D P Phillips,et al.  Effects of bilateral auditory cortical lesions on gap-detection thresholds in the ferret (Mustela putorius). , 1996, Behavioral neuroscience.

[10]  B. Schofield,et al.  Unilateral and bilateral projections from cortical cells to the inferior colliculus in guinea pigs , 2005, Brain Research.

[11]  A R Palmer,et al.  The representation of the spectra and fundamental frequencies of steady-state single- and double-vowel sounds in the temporal discharge patterns of guinea pig cochlear-nerve fibers. , 1990, The Journal of the Acoustical Society of America.

[12]  F. de Ribaupierre,et al.  Corticofugal modulation of the information processing in the auditory thalamus of the cat , 2004, Experimental Brain Research.

[13]  J. Winer Decoding the auditory corticofugal systems , 2005, Hearing Research.

[14]  Larry F Hughes,et al.  GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus , 2002, Hearing Research.

[15]  Igor V Tetko,et al.  Corticofugal modulation of functional connectivity within the auditory thalamus of rat, guinea pig and cat revealed by cooling deactivation , 1999, Journal of Neuroscience Methods.

[16]  E. C. Cherry Some Experiments on the Recognition of Speech, with One and with Two Ears , 1953 .

[17]  N. Weinberger,et al.  Corticofugal modulation of the medial geniculate body , 1976, Experimental Neurology.

[18]  B. Schofield,et al.  Projections to the inferior colliculus from layer VI cells of auditory cortex , 2009, Neuroscience.

[19]  Stephen G. Lomber,et al.  The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function , 1999, Journal of Neuroscience Methods.

[20]  A. R. Palmer,et al.  Some investigations into non-passive listening , 2007, Hearing Research.

[21]  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.

[22]  C. Maggi,et al.  Suitability of urethane anesthesia for physiopharmacological investigations. Part 3: Other systems and conclusions , 1986, Experientia.

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

[24]  T. Yamakura,et al.  Different sensitivities of NMDA receptor channel subtypes to non-competitive antagonists. , 1993, Neuroreport.

[25]  J. Kelly,et al.  Detection of sinusoidal amplitude modulated sounds: Deficits after bilateral lesions of auditory cortex in the rat , 2007, Hearing Research.

[26]  D. Sinex,et al.  Responses of inferior colliculus neurons to double harmonic tones. , 2007, Journal of neurophysiology.

[27]  R. Carlyon Encoding the fundamental frequency of a complex tone in the presence of a spectrally overlapping masker. , 1996, The Journal of the Acoustical Society of America.

[28]  R. Carlyon,et al.  The role of resolved and unresolved harmonics in pitch perception and frequency modulation discrimination. , 1994, The Journal of the Acoustical Society of America.

[29]  Alain de Cheveigné,et al.  Pitch perception models , 2005 .

[30]  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.

[31]  W. K. Taylor,et al.  Some Further Experiments upon the Recognition of Speech, with One and with Two Ears , 1954 .

[32]  I. Nelken,et al.  Neurons and Objects: The Case of Auditory Cortex , 2008, Front. Neurosci..

[33]  E. Bertaccini,et al.  Anesthetics and ion channels: molecular models and sites of action. , 2001, Annual review of pharmacology and toxicology.

[34]  T. Yamakura,et al.  Subunit-dependent Inhibition of Human Neuronal Nicotinic Acetylcholine Receptors and Other Ligand-gated Ion Channels by Dissociative Anesthetics Ketamine and Dizocilpine , 2000, Anesthesiology.

[35]  E. Eger,et al.  Actions of fluorinated alkanols on GABA(A) receptors: relevance to theories of narcosis. , 1999, Anesthesia and analgesia.

[36]  Alan R Palmer,et al.  Descending projections from auditory cortex modulate sensitivity in the midbrain to cues for spatial position. , 2008, Journal of neurophysiology.

[37]  Hubert H. Lim,et al.  Antidromic activation reveals tonotopically organized projections from primary auditory cortex to the central nucleus of the inferior colliculus in guinea pig. , 2007, Journal of neurophysiology.

[38]  Alan R. Palmer,et al.  Identification and localisation of auditory areas in guinea pig cortex , 2000, Experimental Brain Research.

[39]  T. Griffiths,et al.  What is an auditory object? , 2004, Nature Reviews Neuroscience.

[40]  E D Young,et al.  The representation of concurrent vowels in the cat anesthetized ventral cochlear nucleus: evidence for a periodicity-tagged spectral representation. , 1997, The Journal of the Acoustical Society of America.

[41]  M. Kubovy,et al.  Auditory and visual objects , 2001, Cognition.

[42]  J. Kelly,et al.  Contribution of AMPA, NMDA, and GABAA Receptors to Temporal Pattern of Postsynaptic Responses in the Inferior Colliculus of the Rat , 2004, The Journal of Neuroscience.

[43]  Joshua G. W. Bernstein,et al.  Detection and F0 discrimination of harmonic complex tones in the presence of competing tones or noise. , 2006, The Journal of the Acoustical Society of America.

[44]  R. Carlyon,et al.  Masker asynchrony impairs the fundamental-frequency discrimination of unresolved harmonics. , 1996, The Journal of the Acoustical Society of America.

[45]  A. Bregman Auditory Scene Analysis , 2008 .

[46]  E. Eger,et al.  Actions of Fluorinated Alkanols on GABAA Receptors , 1999 .

[47]  J. Popelář,et al.  Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex. , 2003, Physiological research.

[48]  S. Shamma On the Emergence and Awareness of Auditory Objects , 2008, PLoS biology.

[49]  Sophie K Scott,et al.  Auditory processing — speech, space and auditory objects , 2005, Current Opinion in Neurobiology.

[50]  W. Yost Auditory image perception and analysis: The basis for hearing , 1991, Hearing Research.