Paper

Auditory processing remains sensitive to environmental experience during adolescence

Sanes, Dan H, Hotz, Robert A, Anbuhl, Kelsey L, Yao, Justin D, Mowery, Todd M

2021,2022

Overview

Development is a time of great opportunity. A heightened period of neural plasticity contributes to dramatic improvements in perceptual, motor, and cognitive skills. However, developmental plasticity poses a risk: greater malleability of neural circuits exposes them to environmental factors that may impede behavioral maturation. While these risks are well-established prior to sexual maturity (i.e., critical periods), the degree of neural vulnerability during adolescence remains uncertain. To address this question, we induced a transient period of hearing loss (HL) spanning adolescence in the gerbil, confirmed by assessment of circulating sex hormones, and asked whether behavioral and neural deficits are diminished. Wireless recordings were obtained from auditory cortex neurons during perceptual task performance, and within-session behavioral and neural sensitivity were compared. We found that a transient period of adolescent HL caused a significant perceptual deficit (i.e., amplitude modulation detection thresholds) that could be attributed to degraded auditory cortex processing, as confirmed with both single neuron and population-level analyses. To determine whether degraded auditory cortex encoding was attributable to an intrinsic change, we obtained auditory cortex brain slices from adolescent HL animals, and recorded synaptic and discharge properties from auditory cortex pyramidal neurons. There was a clear and novel phenotype, distinct from critical period HL: excitatory postsynaptic potential amplitudes were elevated in adolescent HL animals, whereas inhibitory postsynaptic potentials were unchanged. This is in contrast to critical period deprivation, where there are large changes to synaptic inhibition. Taken together, these results show that sensory perturbations suffered during adolescence can cause long-lasting behavioral deficits that originate, in part, with a dysfunctional cortical circuit. Competing Interest Statement The authors have declared no competing interest.

• Publisher: Cold Spring Harbor Laboratory Press,Cold Spring Harbor Laboratory
• Subject: Adolescents / Auditory pathways / Brain slice preparation / Child development / Cognition & reasoning / Cognitive ability / Cortex (auditory) / Critical period / Developmental plasticity / Environmental factors / Hearing loss / Information processing / Inhibitory postsynaptic potentials / Motor skill / Neural networks / Neuroplasticity / Neuroscience / Phenotypes / Pyramidal cells / Sex hormones / Sexual maturity / Somatosensory cortex