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. 2024 Mar 7;14(1):5624.
doi: 10.1038/s41598-024-56223-x.

Motor oscillations reveal new correlates of error processing in the human brain

Juliana Yordanova  1 , Michael Falkenstein  2 , Vasil Kolev  3
Affiliations

Motor oscillations reveal new correlates of error processing in the human brain

Juliana Yordanova et al. Sci Rep. .

Abstract

It has been demonstrated that during motor responses, the activation of the motor cortical regions emerges in close association with the activation of the medial frontal cortex implicated with performance monitoring and cognitive control. The present study explored the oscillatory neurodynamics of response-related potentials during correct and error responses to test the hypothesis that such continuous communication would modify the characteristics of motor potentials during performance errors. Electroencephalogram (EEG) was recorded at 64 electrodes in a four-choice reaction task and response-related potentials (RRPs) of correct and error responses were analysed. Oscillatory RRP components at extended motor areas were analysed in the theta (3.5-7 Hz) and delta (1-3 Hz) frequency bands with respect to power, temporal synchronization (phase-locking factor, PLF), and spatial synchronization (phase-locking value, PLV). Major results demonstrated that motor oscillations differed between correct and error responses. Error-related changes (1) were frequency-specific, engaging delta and theta frequency bands, (2) emerged already before response production, and (3) had specific regional topographies at posterior sensorimotor and anterior (premotor and medial frontal) areas. Specifically, the connectedness of motor and sensorimotor areas contra-lateral to the response supported by delta networks was substantially reduced during errors. Also, there was an error-related suppression of the phase stability of delta and theta oscillations at these areas. This synchronization reduction was accompanied by increased temporal synchronization of motor theta oscillations at bi-lateral premotor regions and by two distinctive error-related effects at medial frontal regions: (1) a focused fronto-central enhancement of theta power and (2) a separable enhancement of the temporal synchronization of delta oscillations with a localized medial frontal focus. Together, these observations indicate that the electrophysiological signatures of performance errors are not limited to the medial frontal signals, but they also involve the dynamics of oscillatory motor networks at extended cortical regions generating the movement. Also, they provide a more detailed picture of the medial frontal processes activated in relation to error processing.

Keywords: Brain oscillations; Cognitive control; EEG; Error processing; Performance monitoring; Response-related potentials; Theta/delta.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
(A) Group mean reaction times ± SE for correct and error responses produced with the left and the right hand. (B) Group average mechanograms (upper panel) and electromyograms (EMG, lower panel) of correct and error responses produced with the index and middle fingers of the left and the right hand in two experimental conditions (auditory and visual). A threshold of the mechanogram at 5 N is used to determine movement onset (at 0 ms).
Figure 2
Figure 2
CSD transformed time-domain grand average RRPs for CORRECT and ERROR responses at motor electrodes contra-lateral to the responding hand, C4 and C3. LEFT—left-hand responses; RIGHT—right-hand responses; Response onset at 0 ms. Topography maps of the peak of pre-response negative RRP component (designated by the blue vertical line) are illustrated. The fronto-central (FC), central (C), and centro-parietal regions (CP) used for analysis are designated, with the included electrodes in the left, midline and right areas being marked by asterisks.
Figure 3
Figure 3
Time–frequency decomposition plots of TOTAL POWER, temporal synchronization (PLF), region-specific connectedness (R-PLV), and FCz-guided spatial synchronization (PLV) for right-hand RRPs at the contra-lateral C3 electrode. Response onset at 0 ms. Delta (1–3 Hz) and theta (3.5–7 Hz) TF components are demonstrated.
Figure 4
Figure 4
Theta TF component (3.5–7 Hz) of response-related correct and error potentials elicited by left- and right-hand motor responses (A) Total power, (B) Temporal synchronization (PLF), (C) Region-specific connectedness (regional PLV), (D) FCz-guided synchronization FCz-PLV. Left panel—Extracted theta scales at relevant mid-line, contra-, and ipsi-lateral electrodes (explained in the text); Middle panel – Topography maps for correct, error and error minus correct difference at the time of maximal expression (peak) of the signal at contra-lateral central electrodes; Right panel—Dynamic topography difference maps (error minus correct). Response onset at 0 ms.
Figure 5
Figure 5
Delta TF component (1–3 Hz) of response-related correct and error potentials elicited by left- and right-hand motor responses (A) Total power, (B) Temporal synchronization (PLF), (C) Region-specific connectedness (regional PLV), (D) FCz-guided synchronization FCz-PLV. Left panel – Extracted delta scales at relevant mid-line and contra-lateral electrodes (explanations in the text); Middle panel—Topography maps for correct, error and error minus correct parameter at the time of maximal expression (peak) of the signal at contra-lateral central electrodes the time of maximal expression (signal peak); Right panel—Dynamic topography difference maps (error minus correct). Response onset at 0 ms.
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