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. 2019 Sep 19;10(1):4287.
doi: 10.1038/s41467-019-12205-6.

Activity in the dorsal ACC causes deterioration of sequential motor performance due to anxiety

Gowrishankar Ganesh  1   2 , Takehiro Minamoto  3 , Masahiko Haruno  4   5
Affiliations

Activity in the dorsal ACC causes deterioration of sequential motor performance due to anxiety

Gowrishankar Ganesh et al. Nat Commun. .

Abstract

Performance anxiety can profoundly affect motor performance, even in experts such as professional athletes and musicians. Previously, the neural mechanisms underlying anxiety-induced performance deterioration have predominantly been investigated for individual one-shot actions. Sports and music, however, are characterized by action sequences, where many individual actions are assembled to develop a performance. Here, utilizing a novel differential sequential motor learning paradigm, we first show that performance at the junctions between pre-learnt action sequences is particularly prone to anxiety. Next, utilizing functional magnetic resonance imaging (fMRI), we reveal that performance deterioration at the junctions is parametrically correlated with activity in the dorsal anterior cingulate cortex (dACC). Finally, we show that 1 Hz repetitive transcranial magnetic stimulation of the dACC attenuates the performance deterioration at the junctions. These results demonstrate causality between dACC activity and impairment of sequential motor performance due to anxiety, and suggest new intervention techniques against the deterioration.

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Conflict of interest statement

G.G. and M.H. have filed a patent on the use of brain stimulation as an intervention against performance deterioration due to anxiety. The remaining author declares no competing interests.

Figures

Fig. 1
Fig. 1
Experiment 1. a The participants learnt to press a sequence of circles that appeared one after another on a computer screen in front of them. As part learners, they trained on the first six or four circles in a sequence before training on the remaining circles (see right panel). They then went on to train on the whole 10-circle sequence and finally took an anxiety test on the sequence. Single learners trained only on the whole 10-circle sequence before taking the anxiety test. All sessions included 40 sequence trials. b The press sequence time through the last training trials (white background) and the anxiety test session (yellow background) for part learners (red trace) and single learners (blue trace). The shaded area represents the across participant standard error. The inset figures show the local variation in the standard deviation in the inter-press time aligned with the junction “J” (either after the fourth or sixth circle in a) of the pre-learnt sequences by the part learners. For single learners, J was chosen either after the fourth or sixth circle randomly. Asterisk show a difference in the inset figures that is significant (p < 0.05). c The change of participant behavior in the anxiety test session. The across participant change in the sequence press time is shown in the top panel. The average number of times participants pressed a wrong circle and received an electrical shock in a test session are shown in the middle panel. On each box of the boxplot, the line within the box shows the median, the edges of the box are the 25th and 75th percentiles of the data, and the whiskers show the range of the data points. The change in the inter-press time standard deviation (STD) between the first 20 test trials and the last training session is shown in bottom panel. Error bars in the figure represent standard error. All p values represent paired one-sample tests. We checked for the normality of the datasets using the Shapiro–Wilk test before each comparison. To get the p-values a t-test was used for comparisons when the data groups were normal, and a Wilcoxon signed rank test were used when one or both of the datasets were non-normal (see text for details)
Fig. 2
Fig. 2
Experiment 2: a The participants lay in an fMRI scanner and performed a sequential button-press task in which they pressed three buttons in a sequence guided by a visual cue on the screen above them. b Each participant worked as either a part learner or single learner in sessions of 20 trials as shown. c The number of press misses are shown in the top panel with boxplots. The bottom panel shows the absolute change in the inter-press time standard deviation (STD) near the junction in the anxiety test session. Error bars show standard error. d A parametric event-related general linear model analysis was conducted in which the seventh button in every trial was defined as the junction event, and the inter-press time in every trial at the junction was used as the parametric regressor and contrasted between the part- and single learners. A two-sample t-test demonstrated that activity in the dACC (peak MNI coordinates, [0, 36, 36]) and left and dorsal premotor cortices (peak MNI coordinates, [−48, 8, 42]) was significantly higher in part learners than in single learners (p < 0.05, family-wise-error (FWE) corrected). We used p < 0.0005 uncorrected for display purposes here. e The beta values for part learners were positive (p = 0.00017, one-sample t-test), while those for single learners were negative (p = 0.00010, one-sample t-test), and these values were significantly different (p = 0.00000023, two-sample t-test). f The relationship between differential brain activity and the number of electrical shocks. dACC activity was positively correlated with the number of electrical shocks in part learners (left, R = 0.58, p = 0.016), while the correlation was negative in single learners (right, R = −0.64, p = 0.0054). No correlation with shocks was observed in the left premotor cortex of the same part learners (R = 0.38 and p = 0.14) or single learners (R = 0.11 and p = 0.67). On the boxplots in c and e, the line within the box shows the median, the edges of the box are the 25th and 75th percentiles of the data, and the whiskers show the range of the data points
Fig. 3
Fig. 3
Experiment 3: a All participants participated as part learners. They pressed a button pad as in Experiment 2, but in a sitting position. b They trained on the first six and then next four buttons in the sequence, followed by two training sessions on the entire 10-button sequence, again as in Experiment 2. Half of the participants (TMS part learners) then were stimulated with rTMS to their dACC, and the other half (SHAM part learners) experienced SHAM stimulations for the same period. c The number of press misses are shown in the top panel with boxplots for the SHAM part learners (red plot) and TMS part learners (cyan data). On each box of the boxplot, the line within the box shows the median, the edges of the box are the 25th and 75th percentiles of the data, and the whiskers show the range of the data points. The bottom panel shows the absolute change in the inter-press time standard deviation (STD) near the junction in the anxiety test session. Error bars show standard error. The similarity of plots in Figs. 2c and 3c shows rTMS to the dACC attenuates the effects of anxiety on part learners, making them similar to single learners. All error bars represent standard error. All p values represent two-sample tests. We checked for the normality of the datasets using the Shapiro–Wilk test before each comparison. To get the p values, a t-test was used for comparisons when the data groups were normal, and a Wilcoxon rank-sum test were used when one or both of the datasets were non-normal (see text for details)
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