Gap encoding by parvalbumin-expressing interneurons in auditory cortex

Keller, Clifford H.; Kaylegian, Katherine; Wehr, Michael

doi:10.1152/jn.00911.2017

Cited by 42 publications

(55 citation statements)

References 35 publications

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“…With decreasing gap length, the population of neurons that responds to the post-gap onset decreases. The similarity of encoding post-gap onsets and noise bursts hast already been reported at different levels of the auditory pathway (Guo and Burkard 2002;Keller, Kaylegian, and Wehr 2018). Our data suggest that the detection of GIN does not require complex neural computation.…”

Section: Similarity Of Responses Of Brief Gins and Noise Burstssupporting

confidence: 83%

“…Since cortical inhibition is functionally diminished in aged mice (Martin del Campo, Measor, and Razak 2012), this decrease may affect cortical gap representation as well. Indeed, a subpopulation of cortical inhibitory units has recently been found to be especially strongly modulated by gaps (Keller, Kaylegian, and Wehr 2018). However, this modulation was not specific to GINs but also for onset of noise bursts.Boosting of inhibition may nonspecifically increase signal-to-noise ratios at central stages (Natan et al 2015), thereby improving detectability of brief gaps (Gleich, Hamann, Klump, Kittel, and Strutz 2003) but also similar non-salient targets.…”

Section: Similarity Of Responses Of Brief Gins and Noise Burstsmentioning

confidence: 99%

“…Our data on middle aged mice does not contradict a scenario, in which peripheral and central consequences of aging jointly cause a loss in temporal resolution. Central mechanisms may partly be able to compensate a loss in temporal precision of upstream inputs (Walton, Frisina, and O'Neill 1998;Gleich, Hamann, Klump, Kittel, and Strutz 2003;Kopp-Scheinpflug et al 2011;Anderson and Linden 2016;Keller, Kaylegian, and Wehr 2018. The most popular mouse strain used in auditory research, CBA mice, is commonly regarded as not developing age-related peripheral hearing loss (Zheng, Johnson, and Erway 1999).…”

Section: Aging and Temporal Processing Deficitsmentioning

confidence: 99%

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Ultra-fine temporal resolution in auditory processing is preserved in aged mice without peripheral hearing loss

Osterhagen

Hildebrandt

2018

Preprint

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Age-related hearing loss (presbycusis) is caused by damage to the periphery as well as deterioration of central auditory processing. Gap detection is a paradigm to study age-related temporal processing deficits, which is assumed to be determined primarily by the latter. However, peripheral hearing loss is a strong confounding factor when using gap detection to measure temporal processing. In this study, we used mice from the CAST line, which is known to maintain excellent peripheral hearing, to rule out any contribution of peripheral hearing loss to gap detection performance. We employed an operant Go/No-go paradigm to obtain psychometric functions of gap in noise (GIN) detection at young and middle age. Besides, we measured auditory brainstem responses (ABR) and multiunit recordings in the auditory cortex (AC) in order to disentangle the processing stages of gap detection. We found detection thresholds around 0.6 ms in all measurement modalities. Detection thresholds did not increase with age. In the ABR, GIN stimuli are coded as onset responses to the noise that follows the gap, strikingly similar to the ABR of noise bursts in silence (NBIS). The simplicity of the neural representation of the gap together with the preservation of detection threshold in aged CAST mice suggests that GIN detection in the mouse is primarily determined by peripheral, not central processing.

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Section: Similarity Of Responses Of Brief Gins and Noise Burstssupporting

confidence: 83%

Section: Similarity Of Responses Of Brief Gins and Noise Burstsmentioning

confidence: 99%

Section: Aging and Temporal Processing Deficitsmentioning

confidence: 99%

See 1 more Smart Citation

Ultra-fine temporal resolution in auditory processing is preserved in aged mice without peripheral hearing loss

Osterhagen

Hildebrandt

2018

Preprint

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“…GABA A receptor blockade results in cortical neuron responses at lower sound levels, to a broader range of sound levels, to a broader range of modulation rates, and to a broader range of stimulus durations (Chen and Jen, 2000;Wang et al, 2002Wang et al, , 2016Razak and Fuzessery, 2009). Specific manipulations of FS parvalbumin-positive interneurons or low threshold spiking somatostatin-positive interneurons, suggest that FS cells provide temporally precise feedforward inhibition to auditory cortical pyramidal neurons (Hamilton et al, 2013;Li et al, 2014Li et al, , 2015Natan et al, 2017;Cai et al, 2018;Keller et al, 2018;Liu et al, 2019). Together, these observations suggest that the strong FS inhibition contributes to the temporal following ability of pyramidal neurons.…”

Section: Relationship Between Synaptic and Behavioral Findingsmentioning

confidence: 99%

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Mowery¹,

Caras²,

Hassan³

et al. 2019

J. Neurosci.

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Transient periods of childhood hearing loss can induce deficits in aural communication that persist long after auditory thresholds have returned to normal, reflecting long-lasting impairments to the auditory CNS. Here, we asked whether these behavioral deficits could be reversed by treating one of the central impairments: reduction of inhibitory strength. Male and female gerbils received bilateral earplugs to induce a mild, reversible hearing loss during the critical period of auditory cortex development. After earplug removal and the return of normal auditory thresholds, we trained and tested animals on an amplitude modulation detection task. Transient developmental hearing loss induced both learning and perceptual deficits, which were entirely corrected by treatment with a selective GABA reuptake inhibitor (SGRI). To explore the mechanistic basis for these behavioral findings, we recorded the amplitudes of GABA A and GABA B receptor-mediated IPSPs in auditory cortical and thalamic brain slices. In hearing loss-reared animals, cortical IPSP amplitudes were significantly reduced within a few days of hearing loss onset, and this reduction persisted into adulthood. SGRI treatment during the critical period prevented the hearing loss-induced reduction of IPSP amplitudes; but when administered after the critical period, it only restored GABA B receptor-mediated IPSP amplitudes. These effects were driven, in part, by the ability of SGRI to upregulate ␣1 subunitdependent GABA A responses. Similarly, SGRI prevented the hearing loss-induced reduction of GABA A and GABA B IPSPs in the ventral nucleus of the medial geniculate body. Thus, by maintaining, or subsequently rescuing, GABAergic transmission in the central auditory thalamocortical pathway, some perceptual and cognitive deficits induced by developmental hearing loss can be prevented.

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“…In parallel, due to less evidence of offset-responsive neurons in anaesthetized animals, OFF cortical responses have received comparably less attention. Yet, OFF responses have been observed in awake animals throughout the auditory pathway, and in the mouse auditory cortex they constitute from 30% to 70% of the responsive neurons (Scholl et al, 2010;Keller et al, 2018;Joachimsthaler et al, 2014;Liu et al, 2019a;Sollini et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Network dynamics underlying OFF responses in the auditory cortex

Bondanelli

Deneux

Bathellier

et al. 2019

Preprint

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Across sensory systems, complex spatio-temporal patterns of neural activity arise following the onset (ON) and offset (OFF) of simple stimuli. While ON responses have been widely studied, the mechanisms generating OFF responses in cortical areas have so far not been fully elucidated. Recent studies have argued that OFF responses reflect strongly transient sensory coding at the population level, suggesting they may be generated by a collective, network mechanism. We examine here the hypothesis that OFF responses are single-cell signatures of network dynamics and propose a simple model that generates transient OFF responses through recurrent interactions. To test this hypothesis, we analyse the responses of large populations of neurons in auditory cortex recorded using two-photon calcium imaging in awake mice passively listening to auditory stimuli. Adopting a population approach, we find that the OFF responses evoked by individual stimuli define trajectories of activity that evolve in low-dimensional neural subspaces. A geometric analysis of the population OFF responses reveals that, across different stimuli, these neural subspaces lie on largely orthogonal dimensions that define low-dimensional transient coding channels. We show that a linear network model with recurrent interactions provides a simple mechanism for the generation of the strong OFF responses observed in auditory cortex, and accounts for the low-dimensionality of the transient channels and their global structure across stimuli. We finally compare the network model with a single-cell mechanism and show that the single-cell model, while explaining some prominent features of the data, does not account for the structure across stimuli captured by the network model.

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Gap encoding by parvalbumin-expressing interneurons in auditory cortex

Cited by 42 publications

References 35 publications

Ultra-fine temporal resolution in auditory processing is preserved in aged mice without peripheral hearing loss

Ultra-fine temporal resolution in auditory processing is preserved in aged mice without peripheral hearing loss

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Network dynamics underlying OFF responses in the auditory cortex

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