Attention is required for canonical brain signature of prediction error despite early encoding of the stimuli

Abstract

Prediction error is a basic component of predictive-coding theory of brain processing. According to the theory, each stage of brain processing of sensory information generates a model of the current sensory input; subsequent input is compared against the model and only if there is a mismatch, a prediction error, is further processing performed. Recently, Smout and colleagues found that a signature of prediction error, the visual (v) mismatch negativity (MMN), for a fundamental property of visual input—its orientation—was absent without endogenous attention on the stimuli. This is remarkable because the weight of evidence for MMNs from audition and vision is that they occur without endogenous attention. To resolve this discrepancy, we conducted an experiment addressing 2 alternative explanations for Smout and colleagues’ finding: that it was from a lack of reproducibility or that participants’ visual systems did not encode the stimuli when attention was on something else. We conducted a similar experiment to that of Smout and colleagues. We showed 21 participants sequences of identically oriented Gabor patches, standards, and, unpredictably, otherwise identical, Gabor patches differing in orientation by ±15°, ±30°, and ±60°, deviants. To test whether participants encoded the orientation of the standards, we varied the number of standards preceding a deviant, allowing us to search for a decrease in activity with the number of repetitions of standards—repetition suppression. We diverted participants’ attention from the oriented stimuli with a central, letter-detection task. We reproduced Smout and colleagues’ finding of no vMMN without endogenous attention, strengthening their finding. We found that our participants showed repetition suppression: They did encode the stimuli preattentively. We also found early processing of deviants. We discuss various explanations why the earlier processing did not extend into the vMMN time window, including low precision of prediction.

Orientation and contrast deviance examined: Contrast effects mimic deviant-related negativity yet neither produce the canonical neural correlate of prediction error

“…Outside of the vMMN time-window, there was some, albeit weak, evidence to suggest the data for the P1 are more likely to distinguish between deviants and controls in the orientation condition only. Comparable differences for well-controlled orientation changes have been reported by Male and O'Shea [62] and Male et al [19]. In the present study, deviance-related differences (i.e., difference between deviant vs. standard-DRN-and deviant vs. control) appear at the site of peak negativity (i.e., negative pole) only.…”

“…The effect is smaller (Cohen's d = -0.403) than found previously (i.e., Cohen's d = 3.378 [19] and Cohen's d = 3.786 [62]. In prior experiments, the Michelson contrast of orientation stimuli was closer to .99 (Experiment 1 [62] and .60 (Experiment 2 [19]. Possibly, the reduced stimulus contrast in this experiment (M = .393) is responsible.…”

“…In the present study, deviance-related differences (i.e., difference between deviant vs. standard-DRN-and deviant vs. control) appear at the site of peak negativity (i.e., negative pole) only. The effect is smaller (Cohen's d = -0.403) than found previously (i.e., Cohen's d = 3.378 [19] and Cohen's d = 3.786 [62]. In prior experiments, the Michelson contrast of orientation stimuli was closer to .99 (Experiment 1 [62] and .60 (Experiment 2 [19].…”

Systematic review and meta‐analysis of the visual mismatch negativity in schizophrenia

“…This component is elicited mainly by oddball tasks that include an unpredicted or deviant visual or auditory stimulus and a standard or frequent one. Thus, this component accurately represents expectation violation and computations between expected and unexpected stimuli (Chennu et al, 2013;Male & O'Shea, 2023). MMN occurs at an early phase of stimuli perception between 100 and 250 ms after the onset of the rare stimulus in the frontal regions for auditory stimuli (Näätänen et al, 2007) and parieto-occipital for visual stimuli (Kimura et al, 2010;Stefanics et al, 2014).…”

“…MMN occurs at an early phase of stimuli perception between 100 and 250 ms after the onset of the rare stimulus in the frontal regions for auditory stimuli (Näätänen et al, 2007) and parieto-occipital for visual stimuli (Kimura et al, 2010;Stefanics et al, 2014). There is evidence that visual mismatch negativity (vMMN) can also be elicited by unexpected changes, similar to auditory mismatch negativity (aMMN), with simple variations such as orientation (Kimura et al, 2010), motion (Kreml aček et al, 2006) or colour (Czigler et al, 2004) or more complex stimuli (Astikainen & Hietanen, 2009;Male & O'Shea, 2023).…”