Predicting grip force amplitude involves circuits in the anterior basal ganglia

Abstract

The ability to grip objects allows us to perform many activities of daily living such as eating and drinking. Lesions to and disorders of the basal ganglia can cause deficits in grip force control. Although the prediction of grip force amplitude is an important component of performing a grip force task, the extant literature suggests that this process may not include the basal ganglia. This study used functional magnetic resonance imaging (fMRI) to explore the functional brain mechanisms underlying the prediction of grip force amplitude. The mean force and duration of force did not vary across prediction levels. As anticipated, the reaction time decreased with the level of grip force predictions. In confirmation of previous studies, the parieto-frontal and cerebellar circuits increased their fMRI signal as grip force predictability increased. In addition, the novel finding was that anterior nuclei in the basal ganglia such as caudate and anterior putamen also had an fMRI signal that increased with the level of grip force prediction. In contrast, the fMRI signal in posterior nuclei of the basal ganglia did not change with the level of prediction. These findings provide new evidence indicating that anterior basal ganglia nuclei are involved in the predictive scaling of precision grip force control. Further, the results provide additional support for the planning and parameterization model of the basal ganglia by demonstrating that specific anterior nuclei of the basal ganglia are involved in planning grip force.

Figure 1

Experimental design for the prediction task. A, shows the general schematic of the experimental block design which was the same in each scan. B-D, the sequence of ten force pulses (each with 2s of force contraction and 1s of rest) within a task block in the 20% level of predictability, 40% level of predictability, and 80% level of predictability. The P above each respective pulse indicates which pulses were predictable during each predictability condition. Note the target bars are blue for the first and sixth reference pulses and green for the other pulses. The target force levels for predictable pulses appear at amplitude levels determined by the rule governing each level of predictability previously learned by the subject.

Figure 2

Behavioral force output performance. A, shows the group mean force output, B shows the group mean duration of force, C shows the group mean reaction time, and D shows the rate of change of force. Each data in Figure 2 represents the average across the 40 pulses (10 pulses in 4 blocks) for each subject, which was then averaged across the 11 subjects in the study. The standard error of the mean is shown at each prediction level.

Figure 3

Brain imaging results in the cortex across prediction level. A, displays the results from the voxel-wise group analysis showing task related activity in cortical areas that include left dorsolateral prefrontal cortex (DLPFC), pre-supplementary motor area (pre-SMA) and SMA. The group activation threshold is at p < 0.05 (corrected). The complete results from the voxel-wise analysis are presented in Table 1. B, shows results from the ROI analysis with percent signal change in the left DLPFC, pre-SMA and SMA. These cortical areas form part of the network that scaled significantly in activation with increases in the level of predictability. The standard error of the mean is shown at each prediction level.

Figure 4

Subcortical brain imaging results across prediction level. A-C, displays the results from the voxel-wise group analysis showing task related activity in subcortical areas that include left caudate, left and right putamen, left and right lobule VI of the cerebellum. The complete results are shown in Table 1. D, depicts results from the ROI analysis with percent signal change in these same areas. These subcortical areas form part of the network that scaled significantly in activation across the levels of predictability. The standard error of the mean is shown at each prediction level.

Figure 5

Posterior basal ganglia activation across prediction level. Displays the results from the ROI analysis with percent signal change as the dependent measure. These subcortical areas of the basal ganglia did not change in signal intensity across the grip prediction level. External globus pallidus (GPe), internal globus pallidus (GPi), and subthalamic nucleus (STN) are shown. The standard error of the mean is shown at each prediction level.