Earliest experience of a relatively rare sound but not a frequent sound causes long term changes in the adult auditory cortex

Abstract

Early sensory experience during the critical period of development is known to alter sensory cortical response properties and organization. We find that the earliest sound driven activity in the mouse auditory cortex (ACX) can be detected before earcanal opening (ECO). How auditory experience at these ages may influence auditory cortical development is unknown. Particularly, subplate neurons (SPNs), involved in sensory thalamocortical maturation, in the auditory cortex, are also found to be driven by sounds at ages before ECO in mice. We find that SPNs are selective to low probability deviant sounds in auditory streams before ECO, more so than thalamo-recipient, layer 4 (L4) neurons and not after ECO. We hypothesize that SPNs with their deviant selectivity can direct development of L4 responses before ECO. Exposing mice before ECO with a rarely occurring tone in a stream of another tone occurring frequently leads to strengthening of cortical representation of the rare tone, but not the frequent tone in the adult. Control exposure experiments with only a frequently occurring tone and also in other developmental age windows corroborate the importance of low probability sounds in auditory development. With a computational network model of known thalamic inputs to SPNs and L4 we explain the observed developmental plasticity. An information theoretic analysis with sparse coding assumptions also predicts the observations. Thus, salient low probability sounds in the earliest auditory environment causes long term changes in the auditory cortex.

Social experience dependent plasticity of mouse song selectivity without that of song components

“…Future studies need to combine more refined behaviour to link sequences with behaviour and further understand encoding and plasticity of their representation at single neuron and network level. Long term as well as rapid alteration of representation of sounds in mouse A1, with experience, like maternity 28,29 , learning based on reward or fear 32,30 , developmental environment 55,73,74 and artificial involvement of subcortical and higher order structures 75,76 have been shown for single tokens of natural as well as artificial sounds. However, our study shows social experience dependent change in selectivity to behaviourally relevant sequences as a whole and not of its parts (Figs.…”

“…We first performed widefield Ca 2+ imaging 55,56 (see Methods) to identify location of A1 with UF 57,58 and other auditory areas 59 (Fig. 5A).…”

Separate functional subnetworks of excitatory neurons show preference to periodic and random sound structures

“…To maximize the information flow across the hierarchy, neural circuits often show adaptation at a local synaptic level (Yaron et al, 2012; Hershenhoren et al, 2014) both in feedforward and recurrent connections. Through the past studies, it is well known that stimuli that have a low probability of occurrence elicit the highest response, and this has been extensively studied as a deviant selectivity (Khouri and Nelken, 2015), oddball selectivity (Camalier et al, 2019; Mehra et al, 2019; Srivastava and Bandyopadhyay, 2020) and Mismatch Negativity (MMN). A characteristic feature that manifests at the level of a single neuron is a stimulus-specific adaptation (SSA), which is defined as the adaptation in the responses on repeated presentation of the same stimuli.…”