Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Abstract

During developmental critical periods, early-life stress (ELS) induces cognitive deficits and alters neural circuitry in regions underlying learning, memory, and attention. Mechanisms underlying critical period plasticity are shared by sensory cortices and these higher neural regions, suggesting that sensory processing may also be vulnerable to ELS. In particular, the perception and auditory cortical encoding of temporally-varying sounds both mature gradually, even into adolescence, providing an extended postnatal window of susceptibility. To examine the effects of ELS on temporal processing, we developed a model of ELS in the Mongolian gerbil, a well-established model for auditory processing. In both male and female animals, ELS induction impaired the behavioral detection of short gaps in sound, which are critical for speech perception. This was accompanied by reduced neural responses to gaps in auditory cortex, the auditory periphery, and auditory brainstem. ELS thus degrades the fidelity of sensory representations available to higher regions, and could contribute to well-known ELS-induced problems with cognition.Significance Statement:In children and animal models, early-life stress (ELS) leads to deficits in cognition, including problems with learning, memory, and attention. Such problems could arise in part from a low-fidelity representation of sensory information available to higher-level neural regions. Here we demonstrate that ELS degrades sensory responses to rapid variations in sound at multiple levels of the auditory pathway, and concurrently impairs perception of these rapidly-varying sounds. As these sound variations are intrinsic to speech, ELS may thus pose a challenge to communication and cognition through impaired sensory encoding.