Post-Error Slowing as a Consequence of Disturbed Low-Frequency Oscillatory Phase Entrainment

Abstract

A common finding across many reaction time tasks is that people slow down on trials following errors, a phenomenon known as post-error slowing. In the present study, we tested a novel hypothesis about the neural mechanism underlying post-error slowing. Recent research has shown that when task-relevant stimuli occur in a rhythmic stream, neuronal oscillations entrain to the task structure, thereby enhancing reaction speed. We hypothesized that under such circumstances post-error slowing results from an error-induced disturbance of this endogenous brain rhythm. To test this hypothesis, we measured oscillatory EEG dynamics while human subjects performed a demanding discrimination task under time pressure. We found that low-frequency neuronal oscillations entrained to the stimulus presentation rhythm, and that the low-frequency phase at stimulus onset predicted the speed of responding. Importantly, we found that this entrainment was disrupted following errors, and that the degree of phase disturbance was closely related to the degree of post-error slowing on the subsequent trial. These results describe a new mechanism underlying behavioral changes following errors.

The accessory stimulus effect is mediated by phasic arousal: A pupillometry study

“…Such an AS-evoked phase reset may be especially beneficial in tasks in which variability in interstimulus intervals prevents spontaneous entrainment of neural rhythms (cf. van den Brink et al, 2014), a notion consistent with the finding of larger AS effects when target onset is less predictable (Hackley et al, 2009;Sanders, 1980). Second, the AS effect on behavior may be mediated by an arousal-related transient increase in neural gain.…”

“…Electrophysiological studies have shown that the momentary phase of neural oscillations at target onset is an important trial‐by‐trial predictor of perceptual and attentional variability (Van Rullen, Busch, Drewes, & Dubois, ). Response errors, which are known to evoke a phasic arousal response (including pupil dilation; Hajcak, McDonald, & Simons, ; Murphy, van Moort, & Nieuwenhuis, ) lead to a phase reset of slow neural oscillations (van den Brink, Wynn, & Nieuwenhuis, ). Therefore, it seems possible that accessory stimuli improve performance by resetting oscillatory phase to an optimal value for processing of an immediately subsequent target (Diederich, Schomburg, & Colonius, ).…”

Global dynamics of selective attention and its lapses in primary auditory cortex

“…While anti-correlations in the fMRI signal have been proposed to be simply an artifactual consequence of global-signal regression 38 , our electrophysiological findings provide confirmation that counterphase modulations of the patterning of neuronal activity do occur in cortical neuronal ensembles on temporal scales that are comparable to the low-frequency fluctuations identified by neuroimaging studies. Alternatively, as a recent study by van den Brink et al 39 demonstrated, periods of “no entrainment” observed in our data could occur following behavioral errors. However, since the overall false alarm rate was low in our study (Fig 1b), and in some trial blocks false alarms did not occur at all, (Fig 3b), this explanation is unlikely.…”

An adaptive orienting theory of error processing

“…In line with these findings, Houtman and Notebaert () found that signal detection performance on a rapid‐serial visual presentation (RSVP) task was significantly impaired if the response to a flanker stimulus presented before the RSVP array was incorrect. Lastly, van den Brink and colleagues (van den Brink, Wynn, & Nieuwenhuis, ) found that errors lead to an interruption of the low‐frequency phase entrainment that is usually observed during the presentation of chronologically regular stimulus material, further supporting the observation that errors can have rapid, adverse effects on ongoing perceptual processes.…”

“…Somewhat notably, the type of task itself does not seem to play a role in whether a study will find a relative increase or a decrease in accuracy after errors. For example, while several studies using the flanker task have found increases in accuracy following errors compared to correct trials (Grutzmann, Endrass, Klawohn, & Kathmann, ; Marco‐Pallares, Camara, Munte, & Rodriguez‐Fornells, ; Pontifex et al, ; Seifert, von Cramon, Imperati, Tittgemeyer, & Ullsperger, ; Strozyk & Jentzsch, ), other studies using the same paradigm have shown either the opposite pattern (Arnstein, Lakey, Compton, & Kleinow, ; Fiehler, Ullsperger, & von Cramon, ; Franken, van Strien, Franzek, & van de Wetering, ) or no difference between the conditions (Moran, Bernat, Aviyente, Schroder, & Moser, ; van den Brink et al, ). The same picture is true for other tasks, with some studies showing post‐error increases in accuracy (Danielmeier et al, ; Dutilh et al, ; Forster & Cho, ; Klein et al, ), some showing decreases (Bombeke, Schouppe, Duthoo, & Notebaert, ; Carp & Compton, ; Houtman & Notebaert, ; Jentzsch & Dudschig, ; Jonker, Seli, Cheyne, & Smilek, ; Notebaert et al, ; Notebaert & Verguts, ; Van der Borght, Braem, Stevens, & Notebaert, ), and some showing no change (e.g., Hajcak et al, ).…”