Premovement activity in the mesocortical system links peak force but not initiation of force generation under incentive motivation

Abstract

Motivation facilitates motor performance; however, the neural substrates of the psychological effects on motor performance remain unclear. We conducted a functional magnetic resonance imaging experiment while human subjects performed a ready-set-go task with monetary incentives. Although subjects were only motivated to respond quickly, increasing the incentives improved not only reaction time but also peak grip force. However, the trial-by-trial correlation between reaction time and peak grip force was weak. Extensive areas in the mesocortical system, including the ventral midbrain (VM) and cortical motor-related areas, exhibited motivation-dependent activity in the premovement "Ready" period when the anticipated monetary reward was displayed. This premovement activity in the mesocortical system correlated only with subsequent peak grip force, whereas the activity in motor-related areas alone was associated with subsequent reaction time and peak grip force. These findings suggest that the mesocortical system linking the VM and motor-related regions plays a role in controlling the peak of force generation indirectly associated with incentives but not the initiation of force generation.

Keywords: force; motor cortex; reaction time; reward; ventral midbrain.

Fig. 1

Incentive ready-set-go task. (a) Trial procedure for the incentive ready-set-go task. In each trial, the subject was asked to prepare to respond when the “ready” cue was presented and to respond to the appearance of the “go” stimulus as quickly as possible. To manipulate motivation, the task was conducted under three conditions corresponding to different monetary reward amounts for fast responses: ¥500 (HR condition), ¥50 (LR condition), and ¥0 (NR condition). ITI, intertrial interval. (b) Mean grip force trajectory in each condition. The grip force trajectories obtained from a representative subject (M.I.) in the three conditions: HR (red), LR (light red), and NR (gray). Lines and shaded areas represent the mean grip force and standard error of the mean, respectively. MVC, maximum voluntary contraction. (c) Motor performance of all subjects. Reaction times (left) significantly decreased in the following order: HR < LR < NG. In addition, peak grip force was significantly greater in the following order: HR > LR > NG. ^***p < 0.001, ^**p < 0.01, and ^*p < 0.05.

Fig. 2

The trial-by-trial relationship between the initiation and the peak of grip force. (a) Trial-by-trial grip force trajectories from a representative subject (M.I.). (b) The latency to the initiation and peak of trial-by-trial responses. Dots represent latencies in each trial. The distribution of the latencies to the initiation and peak are also shown in the right panel. The reaction time (blue) as the latency to initiation was significantly faster than the latency to peak grip force (green). ***p < 0.001. (c) The scatter plot of trial-by-trial reaction time and peak grip force from a representative subject (M.I.). The color of the circles represents the condition: HR (red filled circles), LR (light red open circles), and NR (gray filled circles). (d) Kendall’s correlation coefficients were calculated for each condition and subject. Each circle denotes the correlation coefficient for each subject and condition. The color of the circles indicates significant (gray) and nonsignificant (white) correlations. Bars represent the median correlation coefficient across subjects in each condition: HR (red bars), LR (light red bars), NR (gray bars), and all conditions (black bars). The significance level was set as p < 0.05 for correlational analyses.

Fig. 3

Preparatory activity during the ready period. (a) Mean preparatory activity across all trials. A, anterior; R, right; S, superior; V, ventral. (b) Effect of reward on preparatory activity (i.e. [HR + LR] > NR conditions). (c) the effect of the amount of anticipated monetary reward on preparatory activity (i.e. HR > LR conditions). The first column shows outlines of linear contrasts. The second and third columns show the results from small-volume correction. The regions of interest, which are outlined with white lines, indicate the ventral midbrain (left-most panel; including the bilateral ventral tegmental area, parabrachial pigmented nucleus, and substantia nigra pars compacta) and ventral pallidum (second panel from left), defined by the in vivo atlas of human subcortical brain nuclei (Pauli et al. 2018). The fourth and fifth columns display the results from whole-brain analysis. Outlined regions in the third column represent the nucleus accumbens, caudate, and putamen, defined by the in vivo atlas of human subcortical brain nuclei.

Fig. 4

Parametric modulation of preparatory activity with subsequent motor performance. (a) Outline of parametric modulation analysis. To illustrate the brain regions where preparatory activity was correlated with subsequent motor performance, the contrasts modulated by subsequent peak grip force (green dots) and reaction time (blue dots) were estimated at the display of the “ready” cue. MVC, maximum voluntary contraction. (b) Brain regions showing preparatory activity negatively correlated with subsequent reaction time. A, anterior; R, right; S, superior; V, ventral. (c) Brain regions showing preparatory activity positively correlated with subsequent peak grip force. (b and c) The left columns show the results from small-volume correction. The regions of interest, which are outlined with white lines, indicate the ventral midbrain (left-most panel; including the bilateral ventral tegmental area, parabrachial pigmented nucleus, and substantia nigra pars compacta) and ventral pallidum (second left panel), defined according to the in vivo atlas of human subcortical brain nuclei (Pauli et al. 2018). The right columns show results from the whole-brain analysis. Outlined regions in the third column indicate the nucleus accumbens, caudate, and putamen, as defined in the in vivo atlas of human subcortical brain nuclei.