RT Journal Article
SR Electronic
T1 Auditory processing remains sensitive to environmental experience during adolescence
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2021.04.12.439537
DO 10.1101/2021.04.12.439537
A1 Kelsey L. Anbuhl
A1 Justin D. Yao
A1 Robert A. Hotz
A1 Todd M. Mowery
A1 Dan H. Sanes
YR 2022
UL http://biorxiv.org/content/early/2022/02/08/2021.04.12.439537.abstract
AB 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. In contrast, perceptual deficits did not occur when HL of the same duration was induced in adulthood. 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 diminished adolescent sensory experience can cause long-lasting behavioral deficits that originate, in part, from a dysfunctional cortical circuit.Summary of experimental design and main findings.Competing Interest StatementThe authors have declared no competing interest.(AC)auditory cortex(HL)hearing loss(AM)amplitude modulation(IPSP)inhibitory postsynaptic potential(EPSP)excitatory postsynaptic potential