Literature DB >> 30755494

Neural Variability Limits Adolescent Skill Learning.

Melissa L Caras1, Dan H Sanes2,3,4,5.   

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.
Copyright © 2019 the authors.

Entities:  

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

Mesh:

Year:  2019        PMID: 30755494      PMCID: PMC6462443          DOI: 10.1523/JNEUROSCI.2878-18.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  122 in total

1.  Brain development during childhood and adolescence: a longitudinal MRI study.

Authors:  J N Giedd; J Blumenthal; N O Jeffries; F X Castellanos; H Liu; A Zijdenbos; T Paus; A C Evans; J L Rapoport
Journal:  Nat Neurosci       Date:  1999-10       Impact factor: 24.884

2.  Effects of attention on the reliability of individual neurons in monkey visual cortex.

Authors:  C J McAdams; J H Maunsell
Journal:  Neuron       Date:  1999-08       Impact factor: 17.173

3.  Mechanisms of perceptual learning.

Authors:  B A Dosher; Z L Lu
Journal:  Vision Res       Date:  1999-09       Impact factor: 1.886

4.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study.

Authors:  Elizabeth R Sowell; Doris A Trauner; Anthony Gamst; Terry L Jernigan
Journal:  Dev Med Child Neurol       Date:  2002-01       Impact factor: 5.449

5.  Practising orientation identification improves orientation coding in V1 neurons.

Authors:  A Schoups; R Vogels; N Qian; G Orban
Journal:  Nature       Date:  2001-08-02       Impact factor: 49.962

6.  Learning to see: experience and attention in primary visual cortex.

Authors:  R E Crist; W Li; C D Gilbert
Journal:  Nat Neurosci       Date:  2001-05       Impact factor: 24.884

7.  Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals.

Authors:  Ralph E Beitel; Christoph E Schreiner; Steven W Cheung; Xiaoqin Wang; Michael M Merzenich
Journal:  Proc Natl Acad Sci U S A       Date:  2003-08-26       Impact factor: 11.205

Review 8.  The genetic mediation of individual differences in sensitivity to pain and its inhibition.

Authors:  J S Mogil
Journal:  Proc Natl Acad Sci U S A       Date:  1999-07-06       Impact factor: 11.205

9.  A new view of language acquisition.

Authors:  P K Kuhl
Journal:  Proc Natl Acad Sci U S A       Date:  2000-10-24       Impact factor: 11.205

10.  Age-related improvements in auditory backward and simultaneous masking in 6- to 10-year-old children.

Authors:  D E Hartley; B A Wright; S C Hogan; D R Moore
Journal:  J Speech Lang Hear Res       Date:  2000-12       Impact factor: 2.297

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  6 in total

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Authors:  Elena K Rotondo; Kasia M Bieszczad
Journal:  J Neurosci       Date:  2021-09-20       Impact factor: 6.167

Review 2.  Non-sensory Influences on Auditory Learning and Plasticity.

Authors:  Melissa L Caras; Max F K Happel; Bharath Chandrasekaran; Pablo Ripollés; Sarah M Keesom; Laura M Hurley; Luke Remage-Healey; Lori L Holt; Beverly A Wright
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Review 3.  The relationship between pubertal hormones and brain plasticity: Implications for cognitive training in adolescence.

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4.  Auditory processing remains sensitive to environmental experience during adolescence in a rodent model.

Authors:  Kelsey L Anbuhl; Justin D Yao; Robert A Hotz; Todd M Mowery; Dan H Sanes
Journal:  Nat Commun       Date:  2022-05-24       Impact factor: 17.694

5.  Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception.

Authors:  Todd M Mowery; Melissa L Caras; Syeda I Hassan; Derek J Wang; Jordane Dimidschstein; Gord Fishell; Dan H Sanes
Journal:  J Neurosci       Date:  2019-08-26       Impact factor: 6.709

Review 6.  Educational fMRI: From the Lab to the Classroom.

Authors:  Mohamed L Seghier; Mohamed A Fahim; Claudine Habak
Journal:  Front Psychol       Date:  2019-12-06
  6 in total

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