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Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex

Abstract

We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.

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Figure 1: Experimental design.
Figure 2: Facilitative STRF plasticity in A1.
Figure 3: Receptive field plasticity in sequential contexts: STRF changes in moving from passive state to active detection tasks with changing targets.
Figure 4: Onset and persistence of STRF plasticity.
Figure 5: Relation of behavior to STRF plasticity.

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Acknowledgements

We thank S. Kalluri for assistance with physiological recording, S. Ray for technical assistance in electronics and major contributions in customized software design, and S. Newman and T. Vardi for assistance with training animals. This research was supported in part by a Director of Central Intelligence (DCI) Fellowship and grants from the US National Institutes of Health and Office of Naval Research.

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Correspondence to Jonathan Fritz.

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Supplementary information

Supplementary Note (PDF 207 kb)

Supplementary Audio 1.

Below are 4 examples of TORCs (Temporally Orthogonal Ripple Combinations). Each of the signals is 3 seconds long. The components tones have randomized phases. The signals differ in either the frequency range of the component tones or direction in which the ripples move. TORC1: The component tones vary from 125 Hz to 4000Hz. The modulating ripples are upward moving. (WAV 58 kb)

Supplementary Audio 2.

Below are 4 examples of TORCs (Temporally Orthogonal Ripple Combinations). Each of the signals is 3 seconds long. The components tones have randomized phases. The signals differ in either the frequency range of the component tones or direction in which the ripples move. TORC2: Same as TORC1, but with ripples moving downward. (WAV 58 kb)

Supplementary Audio 3.

Below are 4 examples of TORCs (Temporally Orthogonal Ripple Combinations). Each of the signals is 3 seconds long. The components tones have randomized phases. The signals differ in either the frequency range of the component tones or direction in which the ripples move. TORC3: Same as TORC2, but with components tones varying from 250 Hz to 8000Hz. (WAV 117 kb)

Supplementary Audio 4.

Below are 4 examples of TORCs (Temporally Orthogonal Ripple Combinations). Each of the signals is 3 seconds long. The components tones have randomized phases. The signals differ in either the frequency range of the component tones or direction in which the ripples move. TORC4: Same as TORC2, but with components tones varying from 500 Hz to 16000Hz. (WAV 234 kb)

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Fritz, J., Shamma, S., Elhilali, M. et al. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci 6, 1216–1223 (2003). https://doi.org/10.1038/nn1141

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