Prestimulus alpha power predicts fidelity of sensory encoding in perceptual decision making

doi:10.1016/j.neuroimage.2013.10.041

NeuroImage

Volume 87, 15 February 2014, Pages 242-251

https://doi.org/10.1016/j.neuroimage.2013.10.041 Get rights and content

Highlights

•
Task-related EEG components are identified using a linear multivariate classifier.
•
Prestimulus alpha variability correlates with an early poststimulus component.
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No correlation is seen with a later component linked to evidence accumulation.
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We conclude prestimulus alpha modulates sensory encoding during perceptual decisions.

Abstract

Pre-stimulus α power has been shown to correlate with the behavioral accuracy of perceptual decisions. In most cases, these correlations have been observed by comparing α power for different behavioral outcomes (e.g. correct vs incorrect trials). In this paper we investigate such covariation within the context of behaviorally-latent fluctuations in task-relevant post-stimulus neural activity. Specially we consider variations of pre-stimulus α power with post-stimulus EEG components in a two alternative forced choice visual discrimination task. EEG components, discriminative of stimulus class, are identified using a linear multivariate classifier and only the variability of the components for correct trials (regardless of stimulus class, and for nominally identical stimuli) are correlated with the corresponding pre-stimulus α power. We find a significant relationship between the mean and variance of the pre-stimulus α power and the variation of the trial-to-trial magnitude of an early post-stimulus EEG component. This relationship is not seen for a later EEG component that is also discriminative of stimulus class and which has been previously linked to the quality of evidence driving the decision process. Our results suggest that early perceptual representations, rather than temporally later neural correlates of the perceptual decision, are modulated by pre-stimulus state.

Introduction

Perceptual decision making is often described as the simplest form of a cognitive process, in that it involves transforming sensory evidence into a decision and behavioral response (Gold and Shadlen, 2007, Heekeren et al., 2004, Smith and Ratcliff, 2004). Substantial work has looked to identify and characterize the neural processes underlying perceptual decision making, with a focus on the neural correlates of processes that occur post-stimulus. For instance, experiments in non-human primates have shown neurons in the lateral intraparietal area (LIP) demonstrate activity indicative of evidence accumulation (Gold and Shadlen, 2007, Liu and Pleskac, 2011, Shadlen and Newsome, 2001). Analogous studies using neuroimaging in humans have focused on, among other areas, dorsal lateral prefrontal cortex (dLPFC) functioning as a comparator of decision alternatives (Heekeren et al., 2004, Heekeren et al., 2006, Ostwald et al., 2012, Philiastides et al., 2011).

Not all aspects of a perceptual decision are characterized by the post-stimulus activity. The state of the subject prior to stimulus presentation is also a factor in understanding how the perceptual decision evolves. Several groups have measured pre-stimulus oscillatory activity as a way to index the state of the subject prior to the presentation of the stimulus. Pre-stimulus oscillations in the α band (8–12 Hz) have been shown to correlate with visual discrimination performance (Babiloni et al., 2006, Hanslmayr et al., 2007, Hanslmayr et al., 2011, Thut et al., 2006, Van Dijk et al., 2008). Pre-stimulus α power is hypothesized to reflect top-down control of attention (Wyart and Tallon-Baudry, 2009) with increased pre-stimulus α power representing a low attentional state resulting in reduced decision accuracy. Recent studies have shown a correlation between pre-stimulus α power and subjective rating of attention toward a visual discrimination task (Macdonald et al., 2011). Pre-stimulus α phase has also shown to be predictive of visual awareness and perception (Busch et al., 2009, Mathewson et al., 2009).

Studies using electroencephalography (EEG) and magnetoencephalography (MEG) investigating pre-stimulus α within the context of perceptual decision making typically analyze data with respect to behavioral responses — e.g. segregating correct and error trials and characterizing the difference in the power spectrum or phase distributions (Busch et al., 2009, Van Dijk et al., 2008). Relatively little work has been done to investigate the variation of pre-stimulus α power when there is no difference in behavioral decision performance or when stimuli are nominally identical. It is possible that constituent neural processes are affected by pre-stimulus attentional state, though by the time the decision is made this relation is not observable in behavior or is confounded by other factors.

In this paper we investigate the relationship between pre-stimulus α power and post-stimulus discriminating components in a two alternative forced choice (2-AFC) decision making task. Unique to our approach is that we do not use behavioral data to separate trials for conducting our analyses, instead we investigate how pre-stimulus α power relates to post-stimulus neural components for cases in which the decisions are correct and the stimuli nominally identical.

Section snippets

Subjects, experimental design and data acquisition

Previous work by our group has used EEG to identify the timing of neural components which reflect the constituent processes of perceptual decision making (Philiastides and Sajda, 2006b, Philiastides and Sajda, 2007, Philiastides et al., 2006, Ratcliff et al., 2009, Sajda et al., 2009). In this previous work we identified a set of post-stimulus neural components that reflected, among other processes, an early perceptual component, correlating with sensory evidence, and a late discriminating

Results

We first analyzed the behavioral data to check whether the manipulation of phase coherence in the images significantly affected subjects' accuracy. All subjects were able to correctly identify more than 90% of images in the easiest trials (45% coherence) but performed at approximately chance for the most difficult trials (20% coherence). Results showed that phase coherence level was positively correlated with detection accuracy (p = 1.79 × 10^− 11, t₍₄₆₎ = 8.84), and negatively correlated with reaction

Discussion

Uncovering the neural correlates of a perceptual decision is likely to lead to a better understanding of the neural processes underlying more complex decision making. In this paper we used a simple decision making task to investigate how pre-stimulus activity varies relative to post-stimulus activity which is discriminative of stimulus category. Specifically we found that pre-stimulus α power is reduced for trials with high magnitude (i.e. high absolute value) of the early discriminating

Acknowledgments

This work has been supported by NIH grants MH085092 and EB004730 and ARO grant W911NF-11-1-0219.

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View full text

Prestimulus alpha power predicts fidelity of sensory encoding in perceptual decision making

Highlights

Abstract

Introduction

Section snippets

Subjects, experimental design and data acquisition

Results

Discussion

Acknowledgments

Int. J. Psychophysiol.

Curr. Biol.

J. Neurosci. Methods

Curr. Biol.

Cogn. Brain Res.

Neuron

Neuroimage

Brain Res. Rev.

J. Mem. Lang.

Trends Cogn. Sci.

Brain Res. Rev.

Neuron

Trends Neurosci.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Clin. Neurophysiol.

Curr. Biol.

Trends Cogn. Sci.

Trends Neurosci.

An objective method for measuring face detection thresholds using the sweep steady-state visual evoked response

J. Vis.

Prediction of response speed by anticipatory high-frequency (gamma band) oscillations in the human brain

Hum. Brain Mapp.

Pre- and poststimulus alpha rhythms are related to conscious visual perception: a high-resolution EEG study

Cereb. Cortex

Temporal characteristics of the influence of punishment on perceptual decision making in the human brain

J. Neurosci.

Responses of neurons in macaque MT to stochastic motion signals

Vis. Neurosci.

A relationship between behavioral choice and the visual responses of neurons in macaque MT

Vis. Neurosci.

The brain's default network: anatomy, function, and relevance to disease

Ann. N. Y. Acad. Sci.

The phase of ongoing EEG oscillations predicts visual perception

J. Neurosci.

The persistences of vision

Philos. Trans. R. Soc. Lond. B Biol. Sci.

Brain dynamics underlying the nonlinear threshold for access to consciousness

PLoS Biol.

Temporal characteristics of iconic memory

Nature

Dynamic predictions: oscillations and synchrony in top-down processing

Nat. Rev. Neurosci.

Parieto-occipital similar to 10 Hz activity reflects anticipatory state of visual attention mechanisms

Neuroreport

Modulation of oscillatory neuronal synchronization by selective visual attention

Science

The neural basis of decision making

Annu. Rev. Neurosci.

A general mechanism for perceptual decision-making in the human brain

Nature