Lighter or heavier than predicted: neural correlates of corrective mechanisms during erroneously programmed lifts

Abstract

A central concept in neuroscience is that the CNS signals the sensory discrepancy between the predicted and actual sensory consequences of action. It has been proposed that the cerebellum and parietal cortex are involved in this process. A discrepancy will trigger preprogrammed corrective responses and update the engaged sensorimotor memories. Here we use functional magnetic resonance imaging with an event-related design to investigate the neuronal correlates of such discrepancies. Healthy adults repeatedly lifted an object between their right index fingers and thumbs, and on some lifting trials, the weight of the object was unpredictably changed between light (230 g) and heavy (830 g). Regardless of whether the weight was heavier or lighter than predicted, activity was found in the right inferior parietal cortex (supramarginal gyrus). This suggests that this region is involved in the comparison of the predicted and actual sensory input and the updating of the sensorimotor memories. When the object was lighter or heavier than predicted, two different types of preprogrammed force corrections occurred. There was a slow force increase when the weight of the object was heavier than predicted. This corrective response was associated with activity in the left primary motor and somatosensory cortices. The fast termination of the excessive force when the object was lighter than predicted activated the right cerebellum. These findings show how the parietal cortex, cerebellum, and motor cortex are involved in the signaling of the discrepancy between predicated and actual sensory feedback and the associated corrective mechanisms.

Figure 1.

Behavioral recordings from erroneously programmed lifts with the heavy weight versus adequately programmed lifts (Change to heavier − No change heavy). The grip force (GF), vertical lift force, and grip force rate and vertical position as a function of time for the adjustment to a heavy weight in three single trials are shown. The histograms in the right panels represent mean static grip forces, maximum grip force rates, load phase duration for the heavy weight, and the influences of weight of the preceding trial: heavy (blue) and light (black). For comparison, the light weight preceded with a light weight is also illustrated (orange). The vertical bars at the top of each column gives +1 SD. Data are pooled from all subjects.

Figure 2.

Behavioral recordings form erroneously programmed lifts with the light weight versus adequately programmed lifts (Change to lighter − No change light). The grip force (GF), vertical lift force, and grip force rate and vertical position as a function of time for the adjustment to a light weight in three single trials are shown. The histograms in the right panels represent mean static grip forces, maximum grip force rates, and load phase duration for the light weight and the influences of weight of the preceding trial: heavy (black) and light (blue). For comparison, the heavy weight preceded with a heavy weight is also illustrated (orange). The vertical bars at the top of each column give +1 SD. Data are pooled from all subjects.

Figure 3.

Areas activated when the weight of the object was unpredictably changed, regardless of whether it was lighter or heavier than predicted. We tested the main effect of change in object weight [(Change to heavier − No change heavy) + (Change to lighter − No change light); p < 0.05 corrected]. Activity was found in the right supramarginal gyrus right (R. Supramarginal g.) of the posterior parietal lobe (right; p < 0.01 corrected) as shown on a coronal (left). The activations are superimposed on a mean image of the participants’ structural scans. For illustrative purposes, we used p < 0.001 uncorrected and >5 voxels to threshold the statistical parametric maps. L, Left hemisphere; R, right hemisphere. The coordinate in standard space for the two slices is indicated. In the right panel, we plot the BOLD response in terms of the contrast estimates from the right supramarginal gyrus (R. SMG) for the two contrasts, (Change to heavier − No change heavy) and (Change to lighter − No change light). As can be seen, there is stronger activity during both types of lifts with unpredictable weight changes compared with the well programmed lifts. a.u., Arbitrary units.

Figure 4.

Neural activity in erroneously programmed trials specific for one type of prestructured force response. A, The primary motor cortex was more strongly activated on lifts performed with a heavy weight, but programmed for a lighter weight, compared with lifts performed with a light weight, but programmed for a heavier weight [(Change to heavier − No change heavy) − (Change to lighter − No change light); p < 0.05 corrected]. B, The right lateral cerebellum (R. Cerebellum; lobule VI/crus I) showed greater activity on lifts performed with a light weight, but programmed for a heavier weight, than on trials performed with a heavy weight, but programmed for a lighter weight [(Change to lighter − No change light) − (Change to heavier − No change heavy); p < 0.05 corrected]. For illustrative purposes, we used p < 0.001 uncorrected and >5 voxels to threshold the statistical parametric maps. The coordinate in standard space for the two slices is indicated. In the bottom panels, we plot the contrast estimates for the contrasts (Change to heavier − No change heavy) and (Change to lighter − No change light). Note the opposite pattern of responses in M1 and the right supramarginal cortex. L, Left hemisphere; R, right hemisphere; a.u., arbitrary units.