Prestimulus Oscillatory Activity over Motor Cortex Reflects Perceptual Expectations

Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behavior, 6500 HB, Nijmegen, The Netherlands, Columbia University, Department of Psychology, New York, New York 10027, and Department of Psychology, University of Amsterdam, 1012 ZA, Amsterdam, The Netherlands.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 01/2013; 33(4):1400-10. DOI: 10.1523/JNEUROSCI.1094-12.2013
Source: PubMed


When perceptual decisions are coupled to a specific effector, preparatory motor cortical activity may provide a window into the dynamics of the perceptual choice. Specifically, previous studies have observed a buildup of choice-selective activity in motor regions over time reflecting the integrated sensory evidence provided by visual cortex. Here we ask how this choice-selective motor activity is modified by prior expectation during a visual motion discrimination task. Computational models of decision making formalize decisions as the accumulation of evidence from a starting point to a decision bound. Within this framework, expectation could change the starting point, rate of accumulation, or the decision bound. Using magneto-encephalography in human observers, we specifically tested for changes in the starting point in choice-selective oscillatory activity over motor cortex. Inducing prior expectation about motion direction biased subjects' perceptual judgments as well as the choice-selective motor activity in the 8-30 Hz frequency range before stimulus onset; the individual strength of these behavioral and neural biases were correlated across subjects. In the absence of explicit expectation cues, spontaneous biases in choice-selective activity were evident over motor cortex. These also predicted eventual perceptual choice and were, at least in part, induced by the choice on the previous trial. We conclude that both endogenous and explicitly induced perceptual expectations bias the starting point of decision-related activity, before the accumulation of sensory evidence.

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Available from: Floris P de Lange,
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    • "No beta modulation was observed in trials without such a prediction. Build-up of choice-predictive activity in motor cortex during a perceptual decision-making task is a well-established phenomenon (Donner et al. 2009) and can also be elicited by prior sensory expectations (de Lange et al. 2013). Because we observed a clear dissociation between fast and slow responses, we believe that the proper interpretation of the beta-band modulation here is as a reflection of an actively generated top-down prediction or expectation . "
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    ABSTRACT: The speed of visual search depends on bottom-up stimulus features (e.g., we quickly locate a red item among blue distractors), but it is also facilitated by the presence of top-down perceptual predictions about the item. Here, we identify the nature, source, and neuronal substrate of the predictions that speed up resumed visual search. Human subjects were presented with a visual search array that was repeated up to 4 times, while brain activity was recorded using magnetoencephalography (MEG). Behaviorally, we observed a bimodal reaction time distribution for resumed visual search, indicating that subjects were extraordinarily rapid on a proportion of trials. MEG data demonstrated that these rapid-response trials were associated with a prediction of (1) target location, as reflected by alpha-band (8-12 Hz) lateralization; and (2) target identity, as reflected by beta-band (15-30 Hz) lateralization. Moreover, we show that these predictions are likely generated in a network consisting of medial superior frontal cortex and right temporo-parietal junction. These findings underscore the importance and nature of perceptual hypotheses for efficient visual search.
    Cerebral Cortex 09/2015; DOI:10.1093/cercor/bhv210 · 8.67 Impact Factor
    • "Consistent with the hypothesis that alpha oscillations enable access to the knowledge system (Klimesch 2012), and that they favor expectation-driven operations over external sensory input (Cooper et al. 2003), we found higher prestimulus alpha oscillations in a supramodal network representing letters when stimuli were predictable, which correlated with visibility on a trial-by-trial basis. These results mesh well with a recent study investigating the effects of prior expectations in motor preparation (de Lange et al. 2013), which also showed that alpha oscillations over occipital sensors were modulated by expectations. In that study, however, predicted and unpredicted cues were not physically matched leaving the question open whether alpha oscillations reflected stimulus differences or expectations. "
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    ABSTRACT: Predictions strongly influence perception. However, the neurophysiological processes that implement predictions remain underexplored. It has been proposed that high- and low-frequency neuronal oscillations act as carriers of sensory evidence and top-down predictions, respectively (von Stein and Sarnthein 2000; Bastos et al. 2012). However, evidence for the latter hypothesis remains scarce. In particular, it remains to be shown whether slow prestimulus alpha oscillations in task-relevant brain regions are stronger in the presence of predictions, whether they influence early categorization processes, and whether this interplay indeed boosts perception. Here, we directly address these questions by manipulating subjects’ prior expectations about the identity of visually presented letters while collecting magnetoencephalographic recordings.We find that predictions lead to increased prestimulus alpha oscillations in a multisensory network representing grapheme/phoneme associations. Furthermore, alpha power interacts with stimulus degradation and top-down expectations to predict visibility ratings, and correlates with the amplitude of early sensory components (P1/N1m complex), suggesting a role in the selective amplification of predicted information. Our results thus indicate that low-frequency alpha oscillations can serve as a mechanism to carry and test sensory predictions about letters.
    Cerebral Cortex 07/2015; DOI:10.1093/cercor/bhv146 · 8.67 Impact Factor
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    • "This activation effectively changes how these features are 'weighted' on the next trial, which yields repetition benefits on subsequent trials that will decay over time. The featureweighting view is intuitive, and the idea that trials can produce 'lingering' activity that affects subsequent performance is supported by several neurophysiological findings (Kristjánsson and Campana, 2010; Yeung et al., 2006; de Lange et al., 2013). Similarly, the idea that such weighting is subject to decay is in line with the observation that facilitation effects have been found to rapidly disappear over the course of some 5–8 trials (Maljkovic and Nakayama, 1994; Hillstrom, 2000), and that long intertrial intervals can attenuate or abolish priming effects (Maljkovic and Nakayama, 2000; Thomson and Milliken, 2012). "
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    ABSTRACT: Memory affects visual search, as is particularly evident from findings that when target features are repeated from one trial to the next, selection is faster. Two views have emerged on the nature of the memory representations and mechanisms that cause these intertrial priming effects: independent feature weighting versus episodic retrieval of previous trials. Previous research has attempted to disentangle these views focusing on short term effects. Here, we illustrate that the episodic retrieval models make the unique prediction of long-term priming: biasing one target type will result in priming of this target type for a much longer time, well after the bias has disappeared. We demonstrate that such long-term priming is indeed found for the visual feature of color, but only in conjunction search and not in singleton search. Two follow-up experiments showed that it was the kind of search (conjunction versus singleton) and not the difficulty, that determined whether long-term priming occurred. Long term priming persisted unaltered for at least 200 trials, and could not be explained as the result of explicit strategy. We propose that episodic memory may affect search more consistently than previously thought, and that the mechanisms for intertrial priming may be qualitatively different for singleton and conjunction search.
    Attention Perception & Psychophysics 04/2015; 77(5). DOI:10.3758/s13414-015-0860-2 · 2.17 Impact Factor
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