Post-stimulatory suppression, facilitation and tuning for delays shape responses of inferior colliculus neurons to sequential pure tones

Temporal changes in the excitability of inferior colliculus (IC) neurons will shape their responses to complex stimuli. Single-unit responses of rat IC neurons to the second (probe) of a pair of tones exhibited suppression, facilitation and delay tuned effects. Responses to probe tones were markedly suppressed (by 76% for contralateral stimulation with equal intensity tone pairs) during contralateral and binaural stimulation in 60% of IC neurons. Suppression developed rapidly as a function of the duration of the initial tone, and approached maximum for tones of less than 200 ms. Suppression decreased as the interval between tones increased, and this recovery of responsiveness was often exponential (time constants: mean: 271.4 ms; median: 72.8 ms; n = 47), and independent of the duration and intensity of preceding stimulation. Facilitation of responses to probe tones was observed chiefly in neurons with 'pauser/buildup' response patterns, and decreased as the intertone interval increased. The greatest suppression of responses to probe tones occurred only after intertone intervals of 32 ms (delayed minimum; n = 8) in 11% of IC neurons. Other IC neurons exhibited an increased excitability to probe tones presented 128 ms after stimulation (delayed maximum; n = 7). The latencies of the later neurons' responses were longer (mean: 29.5 ms) than other IC neurons. The role of suppression in sound localization and echo suppression, and the relationship between 'delay tuning' effects and encoding of complex stimuli are discussed.

[1]  P. Finlayson,et al.  Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing , 1997, Hearing Research.

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

[3]  S. Shore Recovery of forward-masked responses in ventral cochlear nucleus neurons , 1995, Hearing Research.

[4]  T. Furukawa,et al.  Quantal analysis of the size of excitatory post‐synaptic potentials at synapses between hair cells and afferent nerve fibres in goldfish. , 1978, The Journal of physiology.

[5]  J. H. Casseday,et al.  Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. , 1994, Science.

[6]  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.

[7]  Dexter R. F. Irvine,et al.  The Auditory Brainstem: A Review of the Structure and Function of Auditory Brainstem Processing Mechanisms , 1986 .

[8]  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.

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

[10]  L. Aitkin,et al.  The representation of stimulus azimuth by high best-frequency azimuth-selective neurons in the central nucleus of the inferior colliculus of the cat. , 1987, Journal of neurophysiology.

[11]  D. Grantham,et al.  Auditory motion aftereffects , 1979, Perception & psychophysics.

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

[13]  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.

[14]  W H Ehrenstein,et al.  Auditory Aftereffects following Simulated Motion Produced by Varying Interaural Intensity or Time , 1994, Perception.

[15]  J. Blauert Spatial Hearing: The Psychophysics of Human Sound Localization , 1983 .

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

[17]  J. Walsh Depression of excitatory synaptic input in rat striatal neurons , 1993, Brain Research.

[18]  C E Schreiner,et al.  Adaptation and recovery from adaptation in single fiber responses of the cat auditory nerve. , 1991, The Journal of the Acoustical Society of America.

[19]  N. V. Swindale,et al.  Spectral motion produces an auditory after-effect , 1993, Nature.

[20]  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.

[21]  Richard J. Salvi,et al.  Recovery from short-term adaptation in single neurons in the cochlear nucleus , 1990, Hearing Research.

[22]  J. Barker,et al.  Pentobarbitone pharmacology of mammalian central neurones grown in tissue culture. , 1978, The Journal of physiology.

[23]  Joseph P. Walton,et al.  Sensorineural hearing loss alters recovery from short-term adaptation in the C57BL/6 mouse , 1995, Hearing Research.

[24]  P. Finlayson,et al.  Short-term adaptation of excitation and inhibition shapes binaural processing. , 1997, Acta oto-laryngologica.

[25]  J. Kelly,et al.  Sound localization after unilateral lesions of inferior colliculus in the ferret (Mustela putorius). , 1994, Journal of neurophysiology.

[26]  M. Cynader,et al.  The time course of direction-selective adaptation in simple and complex cells in cat striate cortex. , 1993, Journal of neurophysiology.

[27]  L. Trussell,et al.  Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. , 1994, The Journal of physiology.

[28]  M Konishi,et al.  Spatial selectivity and binaural responses in the inferior colliculus of the great horned owl , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Caspary,et al.  Effects of excitant amino acids on acoustic responses of inferior colliculus neurons , 1989, Hearing Research.

[30]  Robert L. Smith,et al.  Forward masking of the compound action potential: Thresholds for the detection of the N1 peak , 1991, Hearing Research.

[31]  J. Watkins,et al.  Evidence for presynaptic depression of monosynaptic excitation in neonatal rat motoneurones by (1S,3S)‐ and (1S,3R)‐ACPD , 1992, Experimental physiology.

[32]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[33]  B M Clopton,et al.  Neural responses in the inferior colliculus of albino rat to binaural stimuli. , 1975, The Journal of the Acoustical Society of America.

[34]  E M Relkin,et al.  Psychophysical and physiological forward masking studies: probe duration and rise-time effects. , 1994, The Journal of the Acoustical Society of America.

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

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

[37]  Günter Ehret,et al.  Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat , 1988, Brain Research Reviews.

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

[39]  Robert P Carlyon,et al.  The development and decline of forward masking , 1988, Hearing Research.

[40]  R M Douglas,et al.  Position-specific adaptation in simple cell receptive fields of the cat striate cortex. , 1991, Journal of neurophysiology.

[41]  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.

[42]  J. Doucet,et al.  Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons , 1991, Hearing Research.

[43]  A. Saul,et al.  Adaptation in single units in visual cortex: The tuning of aftereffects in the temporal domain , 1989, Visual Neuroscience.

[44]  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.

[45]  T. Furukawa,et al.  Adaptive rundown of excitatory post‐synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. , 1978, The Journal of physiology.

[46]  J. Willott,et al.  Responses of inferior colliculus neurons in C57BL/6J mice with and without sensorineural hearing loss: Effects of changing the azimuthal location of a continuous noise masker on responses to contralateral tones , 1994, Hearing Research.

[47]  S Kuwada,et al.  Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat , 1997, The Journal of Neuroscience.

[48]  T. Yin,et al.  Binaural Interaction in the Cat Inferior Colliculus: Physiology and Anatomy , 1980 .

[49]  Adrian Rees,et al.  Responses of neurons in the inferior colliculus of the rat to AM and FM tones , 1983, Hearing Research.

[50]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[51]  R L Smith,et al.  Adaptation, saturation, and physiological masking in single auditory-nerve fibers. , 1979, The Journal of the Acoustical Society of America.

[52]  D. Grantham Motion aftereffects with horizontally moving sound sources in the free field , 1989, Perception & psychophysics.

[53]  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.

[54]  R. Anwyl,et al.  The role of N-methyl-d-aspartate receptors in the generation of short-term potentiation in the rat hippocampus , 1989, Brain Research.