Spike-frequency adaptation in the inferior colliculus.

We investigated spike-frequency adaptation of neurons sensitive to interaural phase disparities (IPDs) in the inferior colliculus (IC) of urethane-anesthetized guinea pigs using a stimulus paradigm designed to exclude the influence of adaptation below the level of binaural integration. The IPD-step stimulus consists of a binaural 3,000-ms tone, in which the first 1,000 ms is held at a neuron's least favorable ("worst") IPD, adapting out monaural components, before being stepped rapidly to a neuron's most favorable ("best") IPD for 300 ms. After some variable interval (1-1,000 ms), IPD is again stepped to the best IPD for 300 ms, before being returned to a neuron's worst IPD for the remainder of the stimulus. Exponential decay functions fitted to the response to best-IPD steps revealed an average adaptation time constant of 52.9 +/- 26.4 ms. Recovery from adaptation to best IPD steps showed an average time constant of 225.5 +/- 210.2 ms. Recovery time constants were not correlated with adaptation time constants. During the recovery period, adaptation to a 2nd best-IPD step followed similar kinetics to adaptation during the 1st best-IPD step. The mean adaptation time constant at stimulus onset (at worst IPD) was 34.8 +/- 19.7 ms, similar to the 38.4 +/- 22.1 ms recorded to contralateral stimulation alone. Individual time constants after stimulus onset were correlated with each other but not with time constants during the best-IPD step. We conclude that such binaurally derived measures of adaptation reflect processes that occur above the level of exclusively monaural pathways, and subsequent to the site of primary binaural interaction.

[1]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[2]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[3]  Alla Borisyuk,et al.  Adaptation and inhibition underlie responses to time-varying interaural phase cues in a model of inferior colliculus neurons. , 2002, Journal of neurophysiology.

[4]  Brian H Scott,et al.  Context-Dependent Adaptive Coding of Interaural Phase Disparity in the Auditory Cortex of Awake Macaques , 2002, The Journal of Neuroscience.

[5]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[6]  Blocking GABAergic Inhibition Increases Sensitivity to Sound Motion Cues in the Inferior Colliculus , 2002, The Journal of Neuroscience.

[7]  Astrid G. Stucke,et al.  Differential modulation of respiratory neuronal discharge patterns by GABA(A) receptor and apamin-sensitive K(+) channel antagonism. , 2001, Journal of neurophysiology.

[8]  M. Kelly,et al.  The noradrenergic inhibition of an apamin-sensitive, small-conductance Ca2+-activated K+ channel in hypothalamic gamma-aminobutyric acid neurons: pharmacology, estrogen sensitivity, and relevance to the control of the reproductive axis. , 2001, The Journal of pharmacology and experimental therapeutics.

[9]  M. Semple,et al.  Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus. , 2001, Journal of neurophysiology.

[10]  Adrienne L. Fairhall,et al.  Efficiency and ambiguity in an adaptive neural code , 2001, Nature.

[11]  R. M. Burger,et al.  Reversible Inactivation of the Dorsal Nucleus of the Lateral Lemniscus Reveals Its Role in the Processing of Multiple Sound Sources in the Inferior Colliculus of Bats , 2001, The Journal of Neuroscience.

[12]  D. Oliver,et al.  Distinct K Currents Result in Physiologically Distinct Cell Types in the Inferior Colliculus of the Rat , 2001, The Journal of Neuroscience.

[13]  D. McAlpine,et al.  A neural code for low-frequency sound localization in mammals , 2001, Nature Neuroscience.

[14]  D McAlpine,et al.  Spatial receptive fields of inferior colliculus neurons to auditory apparent motion in free field. , 2001, Journal of neurophysiology.

[15]  D. Oliver,et al.  Identification of cell types in brain slices of the inferior colliculus , 2000, Neuroscience.

[16]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[17]  P. Pedarzani,et al.  Differential Distribution of Three Ca2+-Activated K+ Channel Subunits, SK1, SK2, and SK3, in the Adult Rat Central Nervous System , 2000, Molecular and Cellular Neuroscience.

[18]  D McAlpine,et al.  Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. , 2000, Journal of neurophysiology.

[19]  J. Kelly,et al.  The commissure of Probst as a source of GABAergic inhibition , 1999, Hearing Research.

[20]  D. Weinreich,et al.  Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  L. Carney,et al.  A model for binaural response properties of inferior colliculus neurons. I. A model with interaural time difference-sensitive excitatory and inhibitory inputs. , 1998, The Journal of the Acoustical Society of America.

[22]  H S Colburn,et al.  A model for binaural response properties of inferior colliculus neurons. II. A model with interaural time difference-sensitive excitatory and inhibitory inputs and an adaptation mechanism. , 1998, The Journal of the Acoustical Society of America.

[23]  M. W. Spitzer,et al.  Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. , 1998, Journal of neurophysiology.

[24]  T. Ishii,et al.  Mechanism of calcium gating in small-conductance calcium-activated potassium channels , 1998, Nature.

[25]  C. Faingold,et al.  In vitro electrophysiology of neurons in subnuclei of rat inferior colliculus , 1998, Hearing Research.

[26]  A. Manira,et al.  Calcium influx through N‐ and P/Q‐type channels activate apamin‐sensitive calcium‐dependent potassium channels generating the late afterhyperpolarization in lamprey spinal neurons , 1998, The European journal of neuroscience.

[27]  M. Semple,et al.  Role of Synaptic Inhibition in Processing of Dynamic Binaural Level Stimuli , 1998, The Journal of Neuroscience.

[28]  T. Sejnowski,et al.  Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. , 1997, Cerebral cortex.

[29]  Laurence O Trussell,et al.  Cellular mechanisms for preservation of timing in central auditory pathways , 1997, Current Opinion in Neurobiology.

[30]  M. Carandini,et al.  A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. , 1997, Science.

[31]  J. Kelly,et al.  Two sources of inhibition affecting binaural evoked responses in the rat's inferior colliculus : the dorsal nucleus of the lateral lemniscus and the superior olivary complex , 1997, Hearing Research.

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

[33]  D. McAlpine,et al.  Interaural delay sensitivity and the classification of low best-frequency binaural responses in the inferior colliculus of the guinea pig , 1996, Hearing Research.

[34]  M. W. Spitzer,et al.  Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. , 1995, Journal of neurophysiology.

[35]  M W Spitzer,et al.  Interaural phase coding in auditory midbrain: influence of dynamic stimulus features. , 1991, Science.

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

[37]  S. Laughlin.  The role of sensory adaptation in the retina. , 1989, The Journal of experimental biology.

[38]  R L Smith,et al.  Conservation of adapting components in auditory-nerve responses. , 1987, The Journal of the Acoustical Society of America.

[39]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[40]  L. A. Westerman,et al.  Rapid adaptation depends on the characteristic frequency of auditory nerve fibers , 1985, Hearing Research.

[41]  Donald Robertson,et al.  Very rapid adaptation in the guinea pig auditory nerve , 1985, Hearing Research.

[42]  B. Hille,et al.  Ionic channels of excitable membranes , 2001 .

[43]  L. A. Westerman,et al.  Rapid and short-term adaptation in auditory nerve responses , 1984, Hearing Research.

[44]  Recovery of eighth nerve action potential thresholds after exposure to short, intense pure tones: similarities with temporary threshold shift , 1983, Hearing Research.

[45]  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.

[46]  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.

[47]  I. Ohzawa,et al.  Contrast gain control in the cat visual cortex , 1982, Nature.

[48]  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.