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Developmental spontaneous activity promotes formation of sensory domains, frequency tuning and proper gain in central auditory circuits.

ABSTRACT: Neurons that process sensory information exhibit bursts of electrical activity during development, providing early training to circuits that will later encode similar features of the external world. In the mammalian auditory system, this intrinsically generated activity emerges from the cochlea prior to hearing onset, but its role in maturation of auditory circuitry remains poorly understood. We show that selective suppression of cochlear supporting cell spontaneous activity disrupts patterned burst firing of central auditory neurons without affecting cell survival or acoustic thresholds. However, neurons in the inferior colliculus of these mice exhibit enhanced acoustic sensitivity and broader frequency tuning, resulting in wider isofrequency laminae. Despite this enhanced neural responsiveness, total tone-responsive regions in the auditory cortex are substantially smaller. Thus, disruption of pre-hearing cochlear activity causes profound changes in neural encoding of sound, with important implications for restoration of hearing in individuals who experience reduced activity during this critical developmental period.

SUBMITTER: Kersbergen CJ

PROVIDER: S-EPMC9730452 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Developmental spontaneous activity promotes formation of sensory domains, frequency tuning and proper gain in central auditory circuits.

Kersbergen Calvin J CJ Babola Travis A TA Rock Jason J Bergles Dwight E DE

Cell reports 20221101 7

Neurons that process sensory information exhibit bursts of electrical activity during development, providing early training to circuits that will later encode similar features of the external world. In the mammalian auditory system, this intrinsically generated activity emerges from the cochlea prior to hearing onset, but its role in maturation of auditory circuitry remains poorly understood. We show that selective suppression of cochlear supporting cell spontaneous activity disrupts patterned b ...[more]

PMID: 36384119

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Project description:Perception of vocalizations and other behaviorally relevant sounds requires integrating acoustic information over hundreds of milliseconds. Sound-evoked activity in auditory cortex typically has much shorter latency, but the acoustic context, i.e., sound history, can modulate sound evoked activity over longer periods. Contextual effects are attributed to modulatory phenomena, such as stimulus-specific adaption and contrast gain control. However, an encoding model that links context to natural sound processing has yet to be established. We tested whether a model in which spectrally tuned inputs undergo adaptation mimicking short-term synaptic plasticity (STP) can account for contextual effects during natural sound processing. Single-unit activity was recorded from primary auditory cortex of awake ferrets during presentation of noise with natural temporal dynamics and fully natural sounds. Encoding properties were characterized by a standard linear-nonlinear spectro-temporal receptive field (LN) model and variants that incorporated STP-like adaptation. In the adapting models, STP was applied either globally across all input spectral channels or locally to subsets of channels. For most neurons, models incorporating local STP predicted neural activity as well or better than LN and global STP models. The strength of nonlinear adaptation varied across neurons. Within neurons, adaptation was generally stronger for spectral channels with excitatory than inhibitory gain. Neurons showing improved STP model performance also tended to undergo stimulus-specific adaptation, suggesting a common mechanism for these phenomena. When STP models were compared between passive and active behavior conditions, response gain often changed, but average STP parameters were stable. Thus, spectrally and temporally heterogeneous adaptation, subserved by a mechanism with STP-like dynamics, may support representation of the complex spectro-temporal patterns that comprise natural sounds across wide-ranging sensory contexts.

Dataset Information

Developmental spontaneous activity promotes formation of sensory domains, frequency tuning and proper gain in central auditory circuits.

Publications

Developmental spontaneous activity promotes formation of sensory domains, frequency tuning and proper gain in central auditory circuits.

Similar Datasets

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