Prediction of human errors by maladaptive changes in event-related brain networks

Abstract

Humans engaged in monotonous tasks are susceptible to occasional errors that may lead to serious consequences, but little is known about brain activity patterns preceding errors. Using functional MRI and applying independent component analysis followed by deconvolution of hemodynamic responses, we studied error preceding brain activity on a trial-by-trial basis. We found a set of brain regions in which the temporal evolution of activation predicted performance errors. These maladaptive brain activity changes started to evolve Ϸ30 sec before the error. In particular, a coincident decrease of deactivation in default mode regions of the brain, together with a decline of activation in regions associated with maintaining task effort, raised the probability of future errors. Our findings provide insights into the brain network dynamics preceding human performance errors and suggest that monitoring of the identified precursor states may help in avoiding human errors in critical real-world situations.deconvolution ͉ performance monitoring ͉ default mode ͉ frontal lobe H uman behavior may be strongly determined by the ongoing intrinsic dynamics of regional brain networks (1-3). Although it is conceivable that patterns of brain activity preceding action execution are causally responsible for the behavioral outcome, previous research of human performance monitoring typically focused on brain activity evoked by and occurring after behavioral errors and the ensuing adaptive compensatory mechanisms (4-6). It is not known yet how far ahead in time the state of cortical brain networks impacts on behavioral performance; some EEG and functional MRI (fMRI) evidence exists suggesting that activity in the preceding trial foreshadows subsequent errors but not earlier than that (7-10). The present study investigated this question by means of a single-trial analysis of event-related independent components (IC) in fMRI data during a visual task requiring rapid responses.We analyzed patterns of evoked brain activity across trials that preceded erroneous behavior and may thus be instrumental in causing errors. Errors in this simple repetitive forced-choice task in a controlled setting may principally have two mutually nonexclusive causes: One source of errors consists simply of random failures to implement the correct behavior, which may be generated by momentary fluctuations in neural activity during stimulus processing and response selection in a given trial (1, 11). Although it is possible to make predictions about adaptive behavior in trials succeeding an error, it would be largely impossible in this condition to anticipate future errors from current brain states. Another possibility is that a proportion of errors may be caused by a systematic maladjustment in cognitive control systems that develops more slowly over time, and which thus affords a prediction about future behavior, in particular the likelihood of an erroneous response from analyzing trends in the history of activity across trials. Models of cognitive control propose a p...

The prestimulus default mode network state predicts cognitive task performance levels on a mental rotation task

“…Previous research investigating the role of the DMN preceding task performance supports our findings that a lower prestimulus DMN state is beneficial for cognitive task performance (Eichele et al., 2008; Esterman et al., 2013; Li et al., 2007; Sali et al., 2016; Soravia et al., 2016; Weissman et al., 2006). In the current study, participants performed the mental rotation task in a sparse event‐related design and were thus not presented with visual input for a longer period.…”

“…In one early study, it was shown that attentional lapses were associated with a higher task‐induced DMN activation on a selective attention task (Weissman et al., 2006). Furthermore, it has been shown that a higher prestimulus DMN activation precedes errors on a go/no‐go task (Li et al., 2007), as well as errors in a Flanker task (Eichele et al., 2008), compared to correct task performance. Since these early studies, prestimulus DMN effects have been investigated more extensively, showing a more differential role of these effects on task performance.…”

“…The abovementioned studies within the cognitive task domain either used cues in order to indicate an approaching trial (Li et al., 2007; Sali et al., 2016) , or employed event‐related designs with relatively short inter‐stimulus periods (Eichele et al., 2008; Esterman et al., 2013; Soravia et al., 2016; Weissman et al., 2006). Thus, participants were externally cued and thereby triggered into a “task state” (for cued paradigms) or had little time to switch this cognitive state (for paradigms with short inter‐trial times).…”

Rapidly acquired multisensory association in the olfactory cortex

“…2008). This method entails estimating the HRF by forming the convolution matrix of the stimulus onsets and multiplying its pseudoinverse with the IC time course.…”

Altered intrinsic organisation of brain networks implicated in attentional processes in adult attention-deficit/hyperactivity disorder: a resting-state study of attention, default mode and salience network connectivity

“…1) were derived from the Automatic Anatomic Labelling (AAL) atlas implemented in the WFU Pickatlas [54][55][56]. After averaging over the relevant voxels, the mean signal time series were extracted from each ROI and were used to create individual ROI-to-ROI connectivity matrices between regions corresponding to DMN, DAN, VAN and SN.…”