Role of the basal ganglia and frontal cortex in selecting and producing internally guided force pulses

Abstract

The basal ganglia comprise a crucial circuit involved in force production and force selection, but the specific role of each nucleus to the production of force pulses and the selection of pulses of different force amplitudes remains unknown. We conducted an fMRI study in which participants produced force using a precision grip while (a) holding a steady-state force, (b) performing a series of force pulses with similar amplitude, and (c) selecting force pulses of different amplitude. Region of interest analyses were conducted in the basal ganglia and frontal cortex to compare percent signal change during force pulse versus steady-state force production and compare force amplitude selection to force production when selection of force amplitude was not present. There were three novel findings in the basal ganglia. First, the caudate nucleus increased activation during the selection of different force amplitudes when compared to producing a series of similar force pulses. Second, GPi, STN, and posterior putamen increased activation during the production of similar force amplitudes when compared to holding a steady-state force, and maintained similar activation during the production of different force amplitudes in which force selection was required. Third, GPe and anterior putamen had increased activation during the production of similar force pulses and further increased activation during the selection of different force pulses. These findings suggest that anterior basal ganglia nuclei are involved in selecting the amplitude of force contractions and posterior basal ganglia nuclei regulate basic aspects of dynamic force pulse production.

Figure 1

Force output time series for hold, similar pulse, and different pulse tasks. Data were obtained from one subject in both externally-guided and internally-guided conditions. During the hold task (upper panel) the subject maintained force output at the level of 15% MVC over the 30-s block. The hold task was used to control for the absolute level of force. During the similar pulse task (middle panel), the subject produced ten force pulses at a constant force level of 15% MVC. Since the force output was specified at 15% MVC, there was no selection of different force amplitudes required for this task. During the different pulse task (lower panel), the subjects produced a series of different force pulses. Therefore, in the internally-guided condition, the subject had to self-select different force amplitudes to accomplish the task.

Figure 2

The group average of force production during the precision grip task is summarized. (A) Mean force is plotted for the externally- and internally-guided hold, similar pulse, and different pulse tasks. (B) Rate of force development is plotted for the externally- and internally-guided hold, similar pulse, and different pulse tasks. (C) Duration of force is plotted for the externally- and internally-guided hold, similar pulse, and different pulse tasks. The error bars represent plus one standard error from the mean. The error bars for the duration of force are present, but they do not appear in the graphs because they are very small.

Figure 3

Results from the group analysis and the regions of interest analysis for the caudate, left anterior cingulate cortex, and the dorsal lateral prefrontal cortex. (A) Depicts axial slices for the hold, similar pulse, and different pulse tasks. Each slice has been masked to focus on the specific region. The activation in each slice is overlaid on the same anatomical brain in Talairach space. The group activation threshold is at p < 0.05 (corrected). (B) Depicts the regions of interest analysis used in our hypothesis testing. Each colored bar represents the percent signal change averaged across subjects and the error bar is plus one standard error of the mean. White is for the hold task, red is the similar pulse task, and blue is the different pulse task. In each of these three brain regions, the percent signal change for the different pulse task which required force selection was significantly higher than that for the similar pulse and hold tasks.

Figure 4

Results from the group analysis and the regions of interest analysis for the GPi, posterior putamen, STN, SMA, and left primary motor cortex. (A) Depicts axial slices for the hold, similar pulse, and different pulse tasks. Each slice has been masked to focus on a specific region. The activation in each slice is overlaid on the same anatomical brain in Talairach space. The group activation threshold is at p < 0.05 (corrected). (B) Depicts the regions of interest analysis used in our hypothesis testing. Each colored bar represents the percent signal change averaged across subjects and the error bar is plus one standard error of the mean. White is for the hold task, red is the similar pulse task, and blue is the different pulse task. In each of these three brain regions, the percent signal change for the similar pulse and different pulse tasks was significantly higher than that for the hold task. However, the percent signal change was not significantly different between the similar pulse and different pulse tasks.

Figure 5

Results from the group analysis and the regions of interest analysis for the external segment of the globus pallidus the anterior putamen, and the left pre-SMA. (A) Depicts axial slices for the hold, similar pulse, and different pulse tasks. Each slice has been masked to focus on a specific region. The activation in each slice is overlaid on the same anatomical brain in Talairach space. The group activation threshold is at p < 0.05 (corrected). (B) Depicts the regions of interest analysis used in our hypothesis testing. Each colored bar represents the percent signal change averaged across subjects and the error bar is plus one standard error of the mean. White is for the hold task, red is the simple pulse task, and blue is the different pulse task. In each of these three brain regions, the percent signal change for the similar pulse task was significantly higher than that for the hold task. Also, the percent signal change for the different pulse task was significantly higher than that in the similar pulse task. The results support progressively greater involvement for both force pulse production and force selection mechanisms in these brain regions.

Figure 6

Percent signal change difference was calculated for different pulse - similar pulse in the externally-guided condition compared to that in the internally-guided condition using t-tests. If the activation were due to the pattern of the force pulse series, we expect an equal increment in the percent signal change in the externally-guided and internally-guided conditions. Alternatively, if the activation in a brain region is selection-related we expected a significantly larger increase in percent signal change during the internally-guided condition where selection (choice) occurred compared to the externally-guided condition where there selection is specified by the external visual stimulus. Caudate, anterior putamen, GPe, DLPFC, ACC, and pre-SMA all had a significant increase in percent signal change in the internal condition in comparison to the external condition. Each bar is the average across ten subjects and the error bar is plus one standard error of the mean.