Passive exposure of adult cats to bandlimited tone pip ensembles or noise leads to long-term response suppression in auditory cortex

Pienkowski, Martin; Munguia, Raymundo; Eggermont, Jos J.

doi:10.1016/j.heares.2011.02.002

Cited by 47 publications

(22 citation statements)

References 40 publications

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“…The first comes from a cortical plasticity perspective. It was recently discovered that even “passive exposure” of adult animals to sounds continuously can induce a persistent suppression of auditory cortical activity evoked by those sounds, possibly as homeostatic compensation for increased afferent activity (Norena et al, 2006; Pienkowski et al, 2011). In our paradigm, cocaring mice hear ultrasonic calls over the ~2 week period of heightened vocalizing during rearing (Haack et al, 1983), so some long-term change seemed likely.…”

Section: Discussionmentioning

confidence: 99%

A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls

et al. 2013

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A growing interest in sensory system plasticity in the natural context of motherhood has created the need to investigate how intrinsic physiological state (e.g., hormonal, motivational, etc.) interacts with sensory experience to drive adaptive cortical plasticity for behaviorally relevant stimuli. Using a maternal mouse model of auditory cortical inhibitory plasticity for ultrasonic pup calls, we examined the role of pup care versus maternal physiological state in the long-term retention of this plasticity. Very recent experience caring for pups by Early Cocarers, which are virgins, produced stronger call-evoked lateral-band inhibition in auditory cortex. However, this plasticity was absent when measured post-weaning in Cocarers, even though it was present at the same time point in Mothers, whose pup experience occurred under a maternal physiological state. A two-alternative choice phonotaxis task revealed that the same animal groups (Early Cocarers and Mothers) demonstrating stronger lateral-band inhibition also preferred pup calls over a neutral sound, a correlation consistent with the hypothesis that this inhibitory mechanism may play a mnemonic role and is engaged to process sounds that are particularly salient. Our electrophysiological data hints at a possible mechanism through which the maternal physiological state may act to preserve the cortical plasticity: selectively suppressing detrimental spontaneous activity in neurons that are responsive to calls, an effect observed only in Mothers. Taken together, the maternal physiological state during the care of pups may help maintain the memory trace of behaviorally salient infant cues within core auditory cortex, potentially ensuring a more rapid induction of future maternal behavior.

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Section: Discussionmentioning

confidence: 99%

A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls

et al. 2013

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“…Galazyuk et al (2014) lengthened the duration of the stimulus to 30 s and observed forward suppression in A1 neurons persisting for 30 s after sound offset, suggesting a scaling of suppression to the duration of masking. In what may be a striking amplification of this principle in normal hearing cats, and Pienkowski et al (2011) found that exposure for 12e24 h/day for 5e16 weeks to moderate-level asynchronous 4e20 kHz tone pips produced a forward suppression of neural responses to the exposure frequencies in A1 that lasted up to several weeks after sound cessation (the time frame of their measurements). This effect was observed to develop within two days in cats that were exposed continuously to tone pips in a pair of third-octave bands centered at 4 and 16 kHz (Pienkowski et al, 2011).…”

Section: Assr Responses In Tinnitus and Rimentioning

confidence: 96%

“…In what may be a striking amplification of this principle in normal hearing cats, and Pienkowski et al (2011) found that exposure for 12e24 h/day for 5e16 weeks to moderate-level asynchronous 4e20 kHz tone pips produced a forward suppression of neural responses to the exposure frequencies in A1 that lasted up to several weeks after sound cessation (the time frame of their measurements). This effect was observed to develop within two days in cats that were exposed continuously to tone pips in a pair of third-octave bands centered at 4 and 16 kHz (Pienkowski et al, 2011). Important for the current findings, forward suppression of spontaneous activity in the exposure band was attended by an increase in neural responsiveness (disinhibition) for frequencies regions above and below the exposure frequencies, possibly as a result of release from lateral inhibition, relative to that in the exposure band where responsiveness was reduced compared to that observed in unexposed control cats Eggermont, 2009, 2012).…”

Section: Assr Responses In Tinnitus and Rimentioning

confidence: 96%

Evidence for differential modulation of primary and nonprimary auditory cortex by forward masking in tinnitus

et al. 2015

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It has been proposed that tinnitus is generated by aberrant neural activity that develops among neurons in tonotopic of regions of primary auditory cortex (A1) affected by hearing loss, which is also the frequency region where tinnitus percepts localize (Eggermont and Roberts 2004; Roberts et al., 2010, 2013). These models suggest (1) that differences between tinnitus and control groups of similar age and audiometric function should depend on whether A1 is probed in tinnitus frequency region (TFR) or below it, and (2) that brain responses evoked from A1 should track changes in the tinnitus percept when residual inhibition (RI) is induced by forward masking. We tested these predictions by measuring (128-channel EEG) the sound-evoked 40-Hz auditory steady-state response (ASSR) known to localize tonotopically to neural sources in A1. For comparison the N1 transient response localizing to distributed neural sources in nonprimary cortex (A2) was also studied. When tested under baseline conditions where tinnitus subjects would have heard their tinnitus, ASSR responses were larger in a tinnitus group than in controls when evoked by 500 Hz probes while the reverse was true for tinnitus and control groups tested with 5 kHz probes, confirming frequency-dependent group differences in this measure. On subsequent trials where RI was induced by masking (narrow band noise centered at 5 kHz), ASSR amplitude increased in the tinnitus group probed at 5 kHz but not in the tinnitus group probed at 500 Hz. When collapsed into a single sample tinnitus subjects reporting comparatively greater RI depth and duration showed comparatively larger ASSR increases after masking regardless of probe frequency. Effects of masking on ASSR amplitude in the control groups were completely reversed from those in the tinnitus groups, with no change seen to 5 kHz probes but ASSR increases to 500 Hz probes even though the masking sound contained no energy at 500 Hz (an "off-frequency" masking effect). In contrast to these findings for the ASSR, N1 amplitude was larger in tinnitus than control groups at both probe frequencies under baseline conditions, decreased after masking in all conditions, and did not relate to RI. These results suggest that aberrant neural activity occurring in the TFR of A1 underlies tinnitus and its modulation during RI. They indicate further that while neural changes occur in A2 in tinnitus, these changes do not reflect the tinnitus percept. Models for tinnitus and forward masking are described that integrate these findings within a common framework.

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“…A large portion of these studies have been performed in cats (Eggermont and Komiya 2000, Pienkowski and Eggermont 2009, Pienkowski and Eggermont 2009, Pienkowski and Eggermont 2010, Pienkowski and Eggermont 2010, Pienkowski, Munguia et al 2011, Pienkowski and Eggermont 2012, Munguia, Pienkowski et al 2013, Pienkowski, Munguia et al 2013). Results from these studies indicate that sound-evoked local field potentials (LFPs), spike discharge rates (SDRs) and spontaneous firing rates in the primary auditory cortex (A1) become hypoactive to sound stimulation within the exposure frequency band (tone-pip ensembles, 68–72 dB SPL) and hyperactive to stimuli near the upper and lower edges of the exposure band (Pienkowski and Eggermont 2010, Pienkowski and Eggermont 2010, Munguia, Pienkowski et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats

et al. 2017

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Prolonged low-level noise exposure alters loudness perception in humans, presumably by decreasing the gain of the central auditory system. Here we test the central gain hypothesis by measuring the acute and chronic physiologic changes at the level of the cochlea and inferior colliculus (IC) after a 75 dB SPL, 10–20 kHz noise exposure for 5 weeks. The compound action potential (CAP) and summating potential (SP) were used to assess the functional status of the cochlea and 16 channel electrodes were used to measure the local field potentials (LFP) and multi-unit spike discharge rates (SDR) from the IC immediately after and one-week post-exposure. Measurements obtained immediately post-exposure demonstrated a significant reduction in supra-threshold CAP amplitudes. In contrast to the periphery, sound-evoked activity in the IC was enhanced in a frequency-dependent manner consistent with models of enhanced central gain. Surprisingly, one-week post-exposure supra-threshold responses from the cochlea had not only recovered, but were significantly larger than normal, and thresholds were significantly better than controls. Moreover, sound-evoked hyperactivity in the IC was sustained within the noise exposure frequency band but suppressed at higher frequencies. When response amplitudes representing the neural output of the cochlea and IC activity at one-week post exposure were compared with control animal responses, a central attenuation phenomenon becomes evident, which may play a key role in understanding why low-level noise can sometimes ameliorate tinnitus and hyperacusis percepts.

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Passive exposure of adult cats to bandlimited tone pip ensembles or noise leads to long-term response suppression in auditory cortex

Cited by 47 publications

References 40 publications

A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls

A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls

Evidence for differential modulation of primary and nonprimary auditory cortex by forward masking in tinnitus

Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats

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