Role of the primary motor and dorsal premotor cortices in the anticipation of forces during object lifting

Abstract

When lifting small objects, people apply forces that match the expected weight of the object. This expectation relies in part on information acquired during a previous lift and on associating a certain weight with a particular object. Our study examined the role of the primary motor and dorsal premotor cortices in predicting weight based either on information acquired during a previous lift (no-cue experiment) or on arbitrary color cues associated with a particular weight (cue experiment). In the two experiments, subjects used precision grip to lift two different weights in a series of trials both before and after we applied low-frequency repetitive transcranial magnetic stimulation over the primary motor and dorsal premotor cortices. In the no-cue experiment, subjects did not receive any previous information about which of two weights they would have to lift. In the cue experiment, a color cue provided information about which of the two weights subjects would have to lift. Our results demonstrate a double dissociation in the effects induced by repetitive stimulation. When applied over the primary motor cortex, repetitive stimulation disrupted the scaling of forces based on information acquired during a previous lift. In contrast, when applied over the dorsal premotor cortex, repetitive stimulation disrupted the scaling of forces based on arbitrary color cues. We conclude that the primary motor and dorsal premotor cortices have unique roles during the anticipatory scaling of forces associated with the lifting of different weights.

Figure 1.

Experimental setup. A illustrates the chronological order of a session. During task performance, subjects performed 21 lifts in which they fixated their gaze on the computer screen until they saw a cue. After cue presentation, they then grasped the manipulandum between the tips of the index finger and thumb and lifted it vertically for a distance of ∼10 cm. They maintained the manipulandum in this position until they saw an arrow pointing down on the computer screen. B illustrates the manipulandum that we used to measure precision grip.

Figure 2.

MEP amplitudes. A, C, Superimposed on magnetic resonance images are projected coil trajectories that indicate estimated locations for induced currents in the brain during repetitive stimulation over the primary motor (M1) and dorsal premotor (PMd) cortices. The brightness of these superimpositions reflects the probability of the coil trajectories. Crosses represent their probabilistic locations. B, D, Overall mean ± SEM MEP amplitudes and MEP amplitudes in the primary motor and dorsal premotor sessions are shown. Asterisks denote significant differences for overall MEP amplitudes (no-cue experiment: ^*p < 0.05 vs 22-20 min before rTMS, 2-0 min before rTMS; ^**p < 0.01 vs 12-10 min before rTMS, 20-22 min after rTMS, 30-32 min after rTMS; cue experiment: ^*p < 0.05 vs 2-0 min before rTMS; ^**p < 0.01 vs 30-32 min after rTMS).

Figure 3.

Grip forces in the no-cue experiment. A represents means ± SEM for the rates in grip force before and after repetitive stimulation over the primary motor cortex (M1). B represents means ± SEM for the rates in grip force before and after repetitive stimulation over the dorsal premotor cortex (PMd). C represents the overall average traces for grip forces 20-12 min before repetitive stimulation over M1. D represents the overall average traces for grip forces 12-20 min after repetitive stimulation over M1. Asterisks denote significant differences between switch conditions (^*p ≤ 0.05; ^**p < 0.01).

Figure 4.

Load forces in the no-cue experiment. A represents means ± SEM for the rates in load force before and after repetitive stimulation over the primary motor cortex (M1). B represents means ± SEM for the load-force times before and after repetitive stimulation over M1. C represents the overall average traces for load forces 20-12 min before repetitive stimulation over M1. D represents the overall average traces for load forces 12-20 min after repetitive stimulation over M1. Asterisks denote significant differences between switch conditions (^*p ≤ 0.05; ^**p < 0.01). Daggers denote significant differences between weight conditions at post-1 (^††p < 0.01).

Figure 5.

Grip forces in the cue experiment. A represents means ± SEM for the rates in grip force before and after repetitive stimulation over the primary motor cortex (M1). B represents means ± SEM for the rates in grip force before and after repetitive stimulation over the dorsal premotor cortex (PMd). C represents the overall average traces for grip forces 20-12 min before repetitive stimulation over PMd. D represents the overall average traces for grip forces 12-20 min after repetitive stimulation over PMd. Asterisks denote significant differences between switch conditions (^*p ≤ 0.05; ^**p < 0.01). Daggers denote significant differences between block conditions (^†p < 0.05 vs pre-2; ^††p < 0.01 vs pre-1 and post-2).

Figure 6.

Load forces in the cue experiment. A represents means ± SEM for the rates in load force before and after repetitive stimulation over the dorsal premotor cortex (PMd). B represents means SEM for the load-force times before and after repetitive stimulation over PMd. C represents the overall average traces for load forces 20-12 min before repetitive stimulation over PMd. D represents the overall average traces for load forces 12-20 min after repetitive stimulation over PMd. Asterisks denote significant differences between switch conditions (^*p ≤ 0.05; ^**p < 0.01).