Earliest Experience of a Relatively Rare Sound But Not a Frequent Sound Causes Long-Term Changes in the Adult Auditory Cortex

Abstract

Sensory experience during a critical period alters sensory cortical responses and organization. We find that the earliest sound-driven activity in the mouse auditory cortex (ACX) starts before ear-canal opening (ECO). The effects of auditory experience before ECO on ACX development are unknown. We find that in mouse ACX subplate neurons (SPNs), crucial in thalamocortical maturation, respond to sounds before ECO showing oddball selectivity. Before ECO, SPNs are more selective to oddball sounds in auditory streams than thalamo-recipient layer 4 (L4) neurons and not after ECO. We hypothesize that SPN's oddball selectivity can direct the development of L4 responses before ECO. Exposing mice, of either sex, before ECO to a rarely occurring tone in a stream of another tone occurring frequently leads to strengthening the adult cortical representation of the rare tone, but not that of the frequent tone. Results of control exposure experiments at multiple developmental windows that also use only a single tone corroborate the observations. We further explain the strengthening of deviant inputs before ECO and not after ECO using a binary network model mimicking the hierarchical structure of subplate and L4 neurons and response properties derived from our data, with synapses following Hebbian spike time-dependent plasticity learning rule. Information-theoretic analysis with sparse coding assumptions also predicts the observations. Thus, relatively salient low probability sounds in the earliest auditory environment cause long-term changes in the ACX.

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 with low probability of occurrence elicit the highest response, and this has been extensively studied as Deviant selectivity (Khouri and Nelken, 2015), oddball selectivity (Camalier et al, 2019;Mehra et al, 2022;Srivastava and Bandyopadhyay, 2020), and mismatch negativity (MMN). An analog of oddball selectivity, stimulus-specific adaptation (SSA), has been extensively studied at the level of single neurons.…”

Prenatal exposure of azadiradione leads to developmental disabilities

“…S-type of calls were more in treated compared to control on P6 and P7 (P < 0.01), while N-types were unchanged on all days except a decrease in treated only on the P5. These ndings indicate that the complex calls numbers are altered in treated animals in compared to controls and this is overlapped with the onset of hearing [35].…”

Editorial: The earliest-born cortical neurons as multi-tasking pioneers: expanding roles for subplate neurons in cerebral cortex organization and function, volume II

“…Transcription factor LHX2 expression in neuronal progenitors of subplate neurons at embryonic day 11.5 is indispensable for correct penetration and pathfinding by thalamocortical axons in the cortical plate (Pal et al, 2021 ). Peripheral sensory stimuli during early postnatal development affect local circuit formation that involves both cortical plate and subplate (Mehra et al, 2022 ; Mukherjee et al, 2022 ; Xue et al, 2022 ).…”