Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing

Finlayson, Paul G.; Adam, Trudy J.

doi:10.1016/s0378-5955(96)00158-x

Cited by 46 publications

(39 citation statements)

References 36 publications

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“…Responses of cortical neurons to binaural stimuli (Reale and Brugge 2000), as well as neurons throughout most of the auditory neuroaxis (Faure et al 2003;Finlayson 1999;Finlayson and Adam 1997;Fitzpatrick et al 1999;Litovsky and Yin 1998b;Yin 1994), can be altered by a preceding sound in a frequency-, level-, and time-dependent manner. The focus of the present study, therefore, is the fluidity of the binaural level response area of cortical neurons.…”

Section: Introductionmentioning

confidence: 99%

Modulation of Level Response Areas and Stimulus Selectivity of Neurons in Cat Primary Auditory Cortex

Zhang

Nakamoto²,

Kitzes³

2005

Journal of Neurophysiology

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Zhang, Jiping, Kyle T. Nakamoto, and Leonard M. Kitzes. Modulation of level response areas and stimulus selectivity of neurons in cat primary auditory cortex. J Neurophysiol 94: 2263-2274, 2005. First published May 25, 2005 10.1152/jn.01207.2004. Sounds commonly occur in sequences, such as in speech. It is therefore important to understand how the occurrence of one sound affects the response to a subsequent sound. We approached this question by determining how a conditioning stimulus alters the response areas of single neurons in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The response areas consisted of responses to stimuli that varied in level at the two ears and delivered at the characteristic frequency of each cell. A binaural conditioning stimulus was then presented Ն50 ms before each of the stimuli comprising the level response area. An effective preceding stimulus alters the shape and severely reduces the size and response magnitude of the level response area. This ability of the preceding stimulus depends on its proximity in the level domain to the level response area, not on its absolute level or on the size of the response it evokes. Preceding stimuli evoke a nonlinear inhibition across the level response area that results in an increased selectivity of a cortical neuron for its preferred binaural stimuli. The selectivity of AI neurons during the processing of a stream of acoustic stimuli is likely to be restricted to a portion of their level response areas apparent in the tone-alone condition. Thus rather than being static, level response areas are fluid; they can vary greatly in extent, shape and response magnitude. The dynamic modulation of the level response area and level selectivity of AI neurons might be related to several tasks confronting the central auditory system. I N T R O D U C T I O NAs acoustic stimuli commonly occur in a temporal relation to other acoustic stimuli, it is important to understand how responses of cortical neurons vary during the processing of a stream of acoustic signals. Throughout the auditory neuroaxis, discharge rate as a function of monaural stimulus level (so called rate-level functions) have been shown to be displaced to higher stimulus levels when stimuli are presented either during or after a conditioning stimulus (Boettcher et

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Section: Introductionmentioning

confidence: 99%

Modulation of Level Response Areas and Stimulus Selectivity of Neurons in Cat Primary Auditory Cortex

Zhang

Nakamoto²,

Kitzes³

2005

Journal of Neurophysiology

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“…SOC neurons receive both ipsilateral and contralateral glycinergic input, with ipsilateral input predominating (Wu and Kelly, 1991, 1994Cant and Hyson, 1992;Grothe and Sanes, 1993;Smith et al, 2000;Brand et al, 2002;Srinivasan et al, 2004). In the LSO the balance between glutamatergic excitation from the cochlear nucleus and glycinergic inhibition is important for detection of interaural level differences (ILD) (Moore and Caspary, 1983;Finlayson and Adam, 1997;Irvine et al, 2001, for reviews). The response of LSO neurons to glycine can be biphasic.…”

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confidence: 99%

Changes in glycine immunoreactivity in the rat superior olivary complex following deafness

et al. 2005

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The balance between inhibitory and excitatory amino acid neurotransmitters contributes to the control of normal functioning of the auditory brainstem. Changes in the level of neuronal activity within the auditory brainstem pathways influence the balance between inhibition and excitation. Activity-dependent plasticity in the auditory pathways can be studied by creating a large decrease in activity through peripheral deafening. Deafness-related decreases in GABA have previously been shown in the inferior colliculus. However, glycine is a more prevalent inhibitory transmitter in the mature superior olivary complex (SOC). The present study therefore examined if there were deafness-related changes in glycine in the SOC using postembedding immunocytochemistry. Animals were bilaterally deafened by an intrascalar injection of neomycin. Five nuclei in the SOC, the lateral superior olive (LSO), superior paraolivary nucleus (SPoN), and the medial, lateral, and ventral nuclei of the trapezoid body (MNTB, LNTB, and VNTB) were examined 14 days following the deafening and compared to normal hearing age-matched controls. The LSO and SPoN were divided into high and low frequency regions. The number of glycine immunoreactive puncta on the somata of principal cells showed significant decreases in all regions assessed, with changes ranging from 50% in the VNTB to 23% in the LSO. J. Comp. Neurol. 494:179-189, 2006. Indexing termsauditory; brainstem; neomycin; superior olivary complex Increases or decreases in activity induce plastic changes in the mature auditory pathways (recently reviewed by Syka, 2002; and more generally by Møller 2001, 2005). There is deafness-associated plasticity at the synaptic level in the mature auditory brainstem, with HHS Public Access Author Manuscript Author ManuscriptAuthor ManuscriptAuthor Manuscript changes in amino acid neurotransmitters and receptors (Bledsoe et al., 1995;Potashner et al., 1997Potashner et al., , 2000Milbrandt et al., 1997;Ryugo et al., 1998;Caspary et al., 1999;Helfert et al., 1999;Mossop et al., 2000;Nakagawa et al., 2000; Sato et al., 2000a,b;Holt et al., 2005), in ion channels (Macica et al., 2003;Lu et al., 2004;von Hehn et al., 2004), as well as in synapse-related proteins such as protein kinases, Gap43, calbindin, ERK, SAPK, NT3 and BDNF (Idrizbegovic et al., 1998;Garcia et al., 2000;Illing and Michler, 2001; Suneja and Potashner, 2003b). Thus, there is a resulting influence on the balance between excitation and inhibition reflected in changes in neuronal response profiles (Bledsoe et al., 1995;Caspary et al., 1995;Francis and Manis, 2000;Kaltenbach and Afman, 2000;Mossop et al., 2000;Salvi et al., 2000;Syka and Rybalko, 2000) as well as in changes in tonotopic maps (Willott et al., 1982(Willott et al., , 1993Robertson and Irvine, 1989;Schwartz et al., 1993;Rajan and Irvine, 1998;Salvi et al., 1999;Nagase et al., 2000). A shift towards decreased inhibition and increased excitation has been reported in the CIC (Vale and Sanes, 2002) associated with decreases in GAB...

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“…Furthermore, electrophysiological studies showed that the binaural response properties in the brainstem (Finlayson and Adam, 1997;Park et al, 2008) and midbrain Semple, 1993, 1998;Sanes et al, 1998;McAlpine et al, 2000;Ingham and McAlpine, 2004;Furukawa et al, 2005;Dahmen et al, 2010;Siveke et al, 2010) depend on preceding sounds. Therefore, adaptation occurs within a few milliseconds ( (3,120) ϭ 3.4, p ϭ 0.036; best IPD, F (3,120) ϭ 3.5, p ϭ 0.034) for the noisebox group compared to control and recovery groups.…”

Section: Comparison With Previous Studiesmentioning

confidence: 99%

“…Adaptation of the underlying neuronal mechanisms at different time scales would help guarantee high spatial acuity during changes in the stimulus statistics of the sound environment, such as increased loudness or background noise. Neurons in the LSO have been shown to adapt their binaural sensitivity depending on sounds that precede the test stimulus by a few milliseconds (Finlayson and Adam, 1997;Park et al, 2008). One mechanism for short-term adaptation of binaural sensitivity is a differential shift in the synaptic weights of excitatory and inhibitory inputs to MSO and LSO via presynaptic GABA B receptor activation (Magnusson et al, 2008;Hassfurth et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Adaptation of Binaural Processing in the Adult Brainstem Induced by Ambient Noise

Siveke

Leibold²,

Schiller³

et al. 2012

J. Neurosci.

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Interaural differences in stimulus intensity and timing are major cues for sound localization. In mammals, these cues are first processed in the lateral and medial superior olive by interaction of excitatory and inhibitory synaptic inputs from ipsi-and contralateral cochlear nucleus neurons. To preserve sound localization acuity following changes in the acoustic environment, the processing of these binaural cues needs neuronal adaptation. Recent studies have shown that binaural sensitivity adapts to stimulation history within milliseconds, but the actual extent of binaural adaptation is unknown. In the current study, we investigated long-term effects on binaural sensitivity using extracellular in vivo recordings from single neurons in the dorsal nucleus of the lateral lemniscus that inherit their binaural properties directly from the lateral and medial superior olives. In contrast to most previous studies, we used a noninvasive approach to influence this processing. Adult gerbils were exposed for 2 weeks to moderate noise with no stable binaural cue. We found monaural response properties to be unaffected by this measure. However, neuronal sensitivity to binaural cues was reversibly altered for a few days. Computational models of sensitivity to interaural time and level differences suggest that upregulation of inhibition in the superior olivary complex can explain the electrophysiological data.

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Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing

Cited by 46 publications

References 36 publications

Modulation of Level Response Areas and Stimulus Selectivity of Neurons in Cat Primary Auditory Cortex

Modulation of Level Response Areas and Stimulus Selectivity of Neurons in Cat Primary Auditory Cortex

Changes in glycine immunoreactivity in the rat superior olivary complex following deafness

Adaptation of Binaural Processing in the Adult Brainstem Induced by Ambient Noise

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