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J Neurosci. 2019 Apr 10;39(15):2889-2902. doi: 10.1523/JNEUROSCI.2878-18.2019. Epub 2019 Feb 12.

Neural Variability Limits Adolescent Skill Learning.

Caras ML1, Sanes DH2,3,4,5.

Author information

1
Center for Neural Science, caras@nyu.edu.
2
Center for Neural Science.
3
Departments of Psychology.
4
Biology, New York University, New York, New York, 10003, and.
5
Neuroscience Institute, NYU Langone Medical Center, New York, New York, 10016.

Abstract

Skill learning is fundamental to the acquisition of many complex behaviors that emerge during development. For example, years of practice give rise to perceptual improvements that contribute to mature speech and language skills. While fully honed learning skills might be thought to offer an advantage during the juvenile period, the ability to learn actually continues to develop through childhood and adolescence, suggesting that the neural mechanisms that support skill learning are slow to mature. To address this issue, we asked whether the rate and magnitude of perceptual learning varies as a function of age as male and female gerbils trained on an auditory task. Adolescents displayed a slower rate of perceptual learning compared with their young and mature counterparts. We recorded auditory cortical neuron activity from a subset of adolescent and adult gerbils as they underwent perceptual training. While training enhanced the sensitivity of most adult units, the sensitivity of many adolescent units remained unchanged, or even declined across training days. Therefore, the average rate of cortical improvement was significantly slower in adolescents compared with adults. Both smaller differences between sound-evoked response magnitudes and greater trial-to-trial response fluctuations contributed to the poorer sensitivity of individual adolescent neurons. Together, these findings suggest that elevated sensory neural variability limits adolescent skill learning.SIGNIFICANCE STATEMENT The ability to learn new skills emerges gradually as children age. This prolonged development, often lasting well into adolescence, suggests that children, teens, and adults may rely on distinct neural strategies to improve their sensory and motor capabilities. Here, we found that practice-based improvement on a sound detection task is slower in adolescent gerbils than in younger or older animals. Neural recordings made during training revealed that practice enhanced the sound sensitivity of adult cortical neurons, but had a weaker effect in adolescents. This latter finding was partially explained by the fact that adolescent neural responses were more variable than in adults. Our results suggest that one mechanistic basis of adult-like skill learning is a reduction in neural response variability.

KEYWORDS:

adolescence; auditory cortex; development; internal noise; perceptual learning; practice

PMID:
30755494
PMCID:
PMC6462443
[Available on 2019-10-10]
DOI:
10.1523/JNEUROSCI.2878-18.2019

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