Spectral plasticity in monkey primary auditory cortex limits performance generalization in a temporal discrimination task.

J Neurophysiol

Department of Otolaryngology-Head and Neck Surgery, University Hospital Magdeburg, Otto-von-Guericke University, Magdeburg, Germany.

Published: December 2020

Auditory experience and behavioral training can modify perceptual performance. However, the consequences of temporal perceptual learning for temporal and spectral neural processing remain unclear. Specifically, the attributes of neural plasticity that underlie task generalization in behavioral performance remain uncertain. To assess the relationship between behavioral and neural plasticity, we evaluated neuronal temporal processing and spectral tuning in primary auditory cortex (AI) of anesthetized owl monkeys trained to discriminate increases in the envelope frequency (e.g., 4-Hz standard vs. >5-Hz targets) of sinusoidally amplitude-modulated (SAM) 1-kHz or 2-kHz carriers. Behavioral and neuronal performance generalization was evaluated for carriers ranging from 0.5 kHz to 8 kHz. Psychophysical thresholds revealed high SAM discrimination acuity for carriers from one octave below to ∼0.6 octave above the trained carrier frequency. However, generalization of SAM discrimination learning progressively declined for carrier frequencies >0.6 octave above the trained carrier frequency. Neural responses in AI showed that SAM discrimination training resulted in ) increases in temporal modulation preference, especially at carriers close to the trained frequency, ) narrowing of spectral tuning for neurons with characteristic frequencies near the trained carrier frequency, potentially limiting spectral generalization of temporal training effects, and ) enhancement of firing-rate contrast for rewarded versus nonrewarded SAM frequencies, providing a potential cue for behavioral temporal discrimination near the trained carrier frequency. Our findings suggest that temporal training at a specific spectral location sharpens local frequency tuning, thus, confining the training effects to a narrow frequency range and limiting generalization of temporal discrimination learning across a wider frequency range. Monkeys' ability to generalize amplitude modulation discrimination to nontrained carriers was limited to one octave below and 0.6 octave above the trained carrier frequency. Asymmetric generalization was paralleled by sharpening in cortical spectral tuning and enhanced firing-rate contrast between rewarded and nonrewarded SAM stimuli at carriers near the trained frequency. The spectral content of the training stimulus specified spectral and temporal plasticity that may provide a neural substrate for limitations in generalization of temporal discrimination learning.

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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864250PMC
http://dx.doi.org/10.1152/jn.00278.2020DOI Listing

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