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Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain

Temporal orienting improves sensory processing, akin to other top–down biases. However, it is unknown whether these improvements reflect increased neural gain to any stimuli presented at expected time points, or specific tuning to task-relevant stimulus aspects. Furthermore, while other top–down bia...

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Autores principales: Auksztulewicz, Ryszard, Myers, Nicholas E., Schnupp, Jan W., Nobre, Anna C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6891052/
https://www.ncbi.nlm.nih.gov/pubmed/31662425
http://dx.doi.org/10.1523/JNEUROSCI.0925-19.2019
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author Auksztulewicz, Ryszard
Myers, Nicholas E.
Schnupp, Jan W.
Nobre, Anna C.
author_facet Auksztulewicz, Ryszard
Myers, Nicholas E.
Schnupp, Jan W.
Nobre, Anna C.
author_sort Auksztulewicz, Ryszard
collection PubMed
description Temporal orienting improves sensory processing, akin to other top–down biases. However, it is unknown whether these improvements reflect increased neural gain to any stimuli presented at expected time points, or specific tuning to task-relevant stimulus aspects. Furthermore, while other top–down biases are selective, the extent of trade-offs across time is less well characterized. Here, we tested whether gain and/or tuning of auditory frequency processing in humans is modulated by rhythmic temporal expectations, and whether these modulations are specific to time points relevant for task performance. Healthy participants (N = 23) of either sex performed an auditory discrimination task while their brain activity was measured using magnetoencephalography/electroencephalography (M/EEG). Acoustic stimulation consisted of sequences of brief distractors interspersed with targets, presented in a rhythmic or jittered way. Target rhythmicity not only improved behavioral discrimination accuracy and M/EEG-based decoding of targets, but also of irrelevant distractors preceding these targets. To explain this finding in terms of increased sensitivity and/or sharpened tuning to auditory frequency, we estimated tuning curves based on M/EEG decoding results, with separate parameters describing gain and sharpness. The effect of rhythmic expectation on distractor decoding was linked to gain increase only, suggesting increased neural sensitivity to any stimuli presented at relevant time points. SIGNIFICANCE STATEMENT Being able to predict when an event may happen can improve perception and action related to this event, likely due to the alignment of neural activity to the temporal structure of stimulus streams. However, it is unclear whether rhythmic increases in neural sensitivity are specific to task-relevant targets, and whether they competitively impair stimulus processing at unexpected time points. By combining magnetoencephalography and encephalographic recordings, neural decoding of auditory stimulus features, and modeling, we found that rhythmic expectation improved neural decoding of both relevant targets and irrelevant distractors presented and expected time points, but did not competitively impair stimulus processing at unexpected time points. Using a quantitative model, these results were linked to nonspecific neural gain increases due to rhythmic expectation.
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spelling pubmed-68910522020-01-16 Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain Auksztulewicz, Ryszard Myers, Nicholas E. Schnupp, Jan W. Nobre, Anna C. J Neurosci Research Articles Temporal orienting improves sensory processing, akin to other top–down biases. However, it is unknown whether these improvements reflect increased neural gain to any stimuli presented at expected time points, or specific tuning to task-relevant stimulus aspects. Furthermore, while other top–down biases are selective, the extent of trade-offs across time is less well characterized. Here, we tested whether gain and/or tuning of auditory frequency processing in humans is modulated by rhythmic temporal expectations, and whether these modulations are specific to time points relevant for task performance. Healthy participants (N = 23) of either sex performed an auditory discrimination task while their brain activity was measured using magnetoencephalography/electroencephalography (M/EEG). Acoustic stimulation consisted of sequences of brief distractors interspersed with targets, presented in a rhythmic or jittered way. Target rhythmicity not only improved behavioral discrimination accuracy and M/EEG-based decoding of targets, but also of irrelevant distractors preceding these targets. To explain this finding in terms of increased sensitivity and/or sharpened tuning to auditory frequency, we estimated tuning curves based on M/EEG decoding results, with separate parameters describing gain and sharpness. The effect of rhythmic expectation on distractor decoding was linked to gain increase only, suggesting increased neural sensitivity to any stimuli presented at relevant time points. SIGNIFICANCE STATEMENT Being able to predict when an event may happen can improve perception and action related to this event, likely due to the alignment of neural activity to the temporal structure of stimulus streams. However, it is unclear whether rhythmic increases in neural sensitivity are specific to task-relevant targets, and whether they competitively impair stimulus processing at unexpected time points. By combining magnetoencephalography and encephalographic recordings, neural decoding of auditory stimulus features, and modeling, we found that rhythmic expectation improved neural decoding of both relevant targets and irrelevant distractors presented and expected time points, but did not competitively impair stimulus processing at unexpected time points. Using a quantitative model, these results were linked to nonspecific neural gain increases due to rhythmic expectation. Society for Neuroscience 2019-12-04 /pmc/articles/PMC6891052/ /pubmed/31662425 http://dx.doi.org/10.1523/JNEUROSCI.0925-19.2019 Text en Copyright © 2019 Auksztulewicz et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Auksztulewicz, Ryszard
Myers, Nicholas E.
Schnupp, Jan W.
Nobre, Anna C.
Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title_full Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title_fullStr Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title_full_unstemmed Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title_short Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain
title_sort rhythmic temporal expectation boosts neural activity by increasing neural gain
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6891052/
https://www.ncbi.nlm.nih.gov/pubmed/31662425
http://dx.doi.org/10.1523/JNEUROSCI.0925-19.2019
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