Prestimulus oscillatory activity over motor cortex reflects perceptual expectations

Abstract

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.

Figure 1.

Spatial localization of oscillatory activity. A, Topography of choice-selective motor lateralization in the 250 ms preceding the response. Topography depicts the spatial distribution of oscillatory lateralization in the low-frequency (8–30 Hz, bottom) and high-frequency range (60–90 Hz, top). B, Topography of motion stimulus-related occipital activity in the period 200–500 ms following the motion stimulus. Topography depicts the spatial distribution of oscillatory activity in the low-frequency (8–30 Hz, bottom) and high-frequency (60–140 Hz, top) ranges. C, Topography of larger low-frequency (7–34 Hz) oscillatory activity when leftward vs rightward motion was expected, in the pre-motion stimulus period (600–0 ms before motion stimulus onset). D, Topography of larger low-frequency (7–15 Hz) oscillatory activity when participants expected versus did not expect a particular motion direction, in the pre-motion stimulus period (1050–100 ms before motion stimulus onset).

Figure 2.

Behavioral results. A, B, Percentage correct (A) and reaction times (B) for trials that were preceded by a valid cue (green), invalid cue (red), or neutral cue (blue), as a function of motion coherence of the stimuli (low, medium, high). C, D, d′ (C) and criterion shift (D) for trials that were preceded by a predictive cue (red) or a neutral cue (blue), as a function of motion coherence of the stimuli (low, medium, high).

Figure 3.

Expectation affects pre-motion stimulus motor-related activity. TFR of motor lateralization (decision signal, quantified as the difference between activity over the left and right sensors overlying the motor cortex; Fig. 1C) as a function of stimulus expectation. A–C, When comparing the decision signal for trials where subjects expect leftward motion (A) with trials when they expect rightward motion (B), there is a large difference in power in low frequencies (C), as early as 600 ms before the onset of the motion stimulus. D, Low-frequency (8–30 Hz) oscillatory activity as a function of expectation and decision. Expectation of leftward motion led to a positive prestimulus bias in the decision signal (red lines), expectation of rightward motion led to a prestimulus negative bias (blue lines). When subjects' expectation was different from the eventual decision (dotted red and blue lines), there was a gradual reversal of decision-related activity after motion stimulus onset. E, Same as D, but for high-frequency (60–90 Hz) oscillatory activity. High-frequency activity dissociated the eventual choice of the subjects, but we did not find any evidence of prestimulus modulation by expectation.

Figure 4.

Spontaneous fluctuations in pre-motion stimulus motor-related activity on neutrally cued trials. TFR of motor lateralization during trials with no explicit expectation. A–C, When comparing the decision signal for neutrally cued trials where subjects decided leftward motion (A) with trials when they decided rightward motion (B), there is a significant pre-motion stimulus lateralization (C), which became significant 250 ms before the onset of the motion stimulus. D, Low-frequency (8–30 Hz) oscillatory activity for neutral trials. Pre-motion stimulus activity (from 250 ms preceding the stimulus) was predictive of eventual choice. E, Same as D, but for high-frequency (60–90 Hz) oscillatory activity.

Figure 5.

Sequential effects on neutrally cued trials. A, Behavioral bias. Percentage of leftward choices on neutrally cued trials as a function of participants' choice on the previous trial and motion coherence on the current trial. B, Neural bias. Prestimulus motor lateralization on neutrally cued trials as a function of participants' choice on the previous trial (red and blue, left and right choice on previous choice respectively) and motion coherence on the current trial.

Figure 6.

Expectation affects prestimulus visual activity. TFR of visual activity (Fig. 1D) as a function of stimulus expectation. A–C, When comparing the decision signal for trials where subjects had an expectation (A) with trials when they had no expectation (B), there is larger occipital power in low frequencies for trials in which subjects had an expectation (C), throughout the prestimulus period. D, Low-frequency (7–15 Hz) oscillatory activity as a function of expectation. E, Same as D, but for high-frequency (60–140 Hz) oscillatory activity.

Figure 7.

Correlation between behavioral and neural markers of expectation. A, Interindividual differences in prestimulus motor lateralization between trials with leftward vs rightward expectation (Fig. 3) correlated with the behaviorally observed criterion shift (Fig. 1D) as a result of the expectation cue. B, Interindividual differences in prestimulus occipital low-frequency power between trials with versus without stimulus expectation (Fig. 4) also correlated with the behaviorally observed criterion shift (Fig. 1D) as a result of the expectation cue.

Figure 8.

Poststimulus motor lateralization reflects integration of perceptual evidence. A, Expected pattern of results. Motor lateralization is expected to increase during the motion stimulus period, with the amount of increase proportional to the strength of the stimulus (motion coherence). B, Observed pattern of results. Motor lateralization increased during the motion stimulus period. Although there was no significant difference in post-motion stimulus motor lateralization as a function of motion coherence, there was a significant difference in preresponse motor lateralization, in line with the expected pattern of results.