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Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment.

ABSTRACT: Predicting the timing of upcoming events enables efficient resource allocation and action preparation. Rhythmic streams, such as music, speech, and biological motion, constitute a pervasive source for temporal predictions. Widely accepted entrainment theories postulate that rhythm-based predictions are mediated by synchronizing low-frequency neural oscillations to the rhythm, as indicated by increased phase concentration (PC) of low-frequency neural activity for rhythmic compared to random streams. However, we show here that PC enhancement in scalp recordings is not specific to rhythms but is observed to the same extent in less periodic streams if they enable memory-based prediction. This is inconsistent with the predictions of a computational entrainment model of stronger PC for rhythmic streams. Anticipatory change in alpha activity and facilitation of electroencephalogram (EEG) manifestations of response selection are also comparable between rhythm- and memory-based predictions. However, rhythmic sequences uniquely result in obligatory depression of preparation-related premotor brain activity when an on-beat event is omitted, even when it is strategically beneficial to maintain preparation, leading to larger behavioral costs for violation of prediction. Thus, while our findings undermine the validity of PC as a sign of rhythmic entrainment, they constitute the first electrophysiological dissociation, to our knowledge, between mechanisms of rhythmic predictions and of memory-based predictions: the former obligatorily lead to resonance-like preparation patterns (that are in line with entrainment), while the latter allow flexible resource allocation in time regardless of periodicity in the input. Taken together, they delineate the neural mechanisms of three distinct modes of preparation: continuous vigilance, interval-timing-based prediction and rhythm-based prediction.

SUBMITTER: Breska A

PROVIDER: S-EPMC5302287 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment.

Breska Assaf A Deouell Leon Y LY

PLoS biology 20170210 2

Predicting the timing of upcoming events enables efficient resource allocation and action preparation. Rhythmic streams, such as music, speech, and biological motion, constitute a pervasive source for temporal predictions. Widely accepted entrainment theories postulate that rhythm-based predictions are mediated by synchronizing low-frequency neural oscillations to the rhythm, as indicated by increased phase concentration (PC) of low-frequency neural activity for rhythmic compared to random strea ...[more]

PMID: 28187128

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Project description:Highlights • Children with and without dyslexia showed consistent phase entrainment.• Dyslexic children had significantly reduced delta band phase consistency.• Dyslexic children had a different preferred phase in delta compared to controls.• The dyslexic brain showed faster pre-stimulus delta band angular velocity. According to the sensory-neural Temporal Sampling theory of developmental dyslexia, neural sampling of auditory information at slow rates (<10 Hz, related to speech rhythm) is atypical in dyslexic individuals, particularly in the delta band (0.5–4 Hz). Here we examine the underlying neural mechanisms related to atypical sampling using a simple repetitive speech paradigm. Fifty-one children (21 control children [15M, 6F] and 30 children with dyslexia [16M, 14F]) aged 9 years with or without developmental dyslexia watched and listened as a ‘talking head’ repeated the syllable “ba” every 500 ms, while EEG was recorded. Occasionally a syllable was “out of time”, with a temporal delay calibrated individually and adaptively for each child so that it was detected around 79.4% of the time by a button press. Phase consistency in the delta (rate of stimulus delivery), theta (speech-related) and alpha (control) bands was evaluated for each child and each group. Significant phase consistency was found for both groups in the delta and theta bands, demonstrating neural entrainment, but not the alpha band. However, the children with dyslexia showed a different preferred phase and significantly reduced phase consistency compared to control children, in the delta band only. Analysis of pre- and post-stimulus angular velocity of group preferred phases revealed that the children in the dyslexic group showed an atypical response in the delta band only. The delta-band pre-stimulus angular velocity (−130 ms to 0 ms) for the dyslexic group appeared to be significantly faster compared to the control group. It is concluded that neural responding to simple beat-based stimuli may provide a unique neural marker of developmental dyslexia. The automatic nature of this neural response may enable new tools for diagnosis, as well as opening new avenues for remediation.

Project description:When presented with complex rhythmic auditory stimuli, humans are able to track underlying temporal structure (e.g., a "beat"), both covertly and with their movements. This capacity goes far beyond that of a simple entrained oscillator, drawing on contextual and enculturated timing expectations and adjusting rapidly to perturbations in event timing, phase, and tempo. Previous modeling work has described how entrainment to rhythms may be shaped by event timing expectations, but sheds little light on any underlying computational principles that could unify the phenomenon of expectation-based entrainment with other brain processes. Inspired by the predictive processing framework, we propose that the problem of rhythm tracking is naturally characterized as a problem of continuously estimating an underlying phase and tempo based on precise event times and their correspondence to timing expectations. We present two inference problems formalizing this insight: PIPPET (Phase Inference from Point Process Event Timing) and PATIPPET (Phase and Tempo Inference). Variational solutions to these inference problems resemble previous "Dynamic Attending" models of perceptual entrainment, but introduce new terms representing the dynamics of uncertainty and the influence of expectations in the absence of sensory events. These terms allow us to model multiple characteristics of covert and motor human rhythm tracking not addressed by other models, including sensitivity of error corrections to inter-event interval and perceived tempo changes induced by event omissions. We show that positing these novel influences in human entrainment yields a range of testable behavioral predictions. Guided by recent neurophysiological observations, we attempt to align the phase inference framework with a specific brain implementation. We also explore the potential of this normative framework to guide the interpretation of experimental data and serve as building blocks for even richer predictive processing and active inference models of timing.

Dataset Information

Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment.

Publications

Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment.

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