The human somatosensory cortex contributes to the encoding of newly learned movements

Abstract

Recent studies have indicated somatosensory cortex involvement in motor learning and retention. However, the nature of its contribution is unknown. One possibility is that the somatosensory cortex is transiently engaged during movement. Alternatively, there may be durable learning-related changes which would indicate sensory participation in the encoding of learned movements. These possibilities are dissociated by disrupting the somatosensory cortex following learning, thus targeting learning-related changes which may have occurred. If changes to the somatosensory cortex contribute to retention, which, in effect, means aspects of newly learned movements are encoded there, disruption of this area once learning is complete should lead to an impairment. Participants were trained to make movements while receiving rotated visual feedback. The primary motor cortex (M1) and the primary somatosensory cortex (S1) were targeted for continuous theta-burst stimulation, while stimulation over the occipital cortex served as a control. Retention was assessed using active movement reproduction, or recognition testing, which involved passive movements produced by a robot. Disruption of the somatosensory cortex resulted in impaired motor memory in both tests. Suppression of the motor cortex had no impact on retention as indicated by comparable retention levels in control and motor cortex conditions. The effects were learning specific. When stimulation was applied to S1 following training with unrotated feedback, movement direction, the main dependent variable, was unaltered. Thus, the somatosensory cortex is part of a circuit that contributes to retention, consistent with the idea that aspects of newly learned movements, possibly learning-updated sensory states (new sensory targets) which serve to guide movement, may be encoded there.

Keywords: cTBS; motor cortex; motor learning; somatosensory cortex.

Fig. 1.

Following a visuomotor adaptation task, participants were tested for retention of learning using either recognition or movement reproduction tests. (A) Experimental apparatus. Participants held the handle of a robot arm and made standard point-to-point reaching movements. An air sled supported the arm. (B) After baseline trials, participants trained with a gradually introduced 30° visuomotor rotation (shown in red). Limited feedback trials are shown with small black ticks. The adaptation task was followed by cTBS stimulation to one of three candidate regions in the brain (M1, S1, and control). Recognition or movement reproduction tests of retention tests were then performed. In tests of movement reproduction, participants were asked to move directly to the remembered position of the target point (dotted line). In recognition tests, the robot moved the participant’s hand in different candidate directions, and they indicated whether this corresponded to their direction of movement (gray line with red markers). (C) cTBS stimulation was applied to M1, S1, or a control zone over the occipital lobe. A representative M1 hot spot is shown with a red dot. A point 2 cm posterior to the M1 hot spot was the stimulation target in S1 (blue dot). (D) Candidate directions in which the robot moved the participants’ hand during recognition tests. (E) Average hand paths during baseline, training, and retention testing. (F) The real-time position of the participant’s hand was shown in full feedback trials. Visual feedback of hand movement direction was gradually rotated in a clockwise direction over the course of training. Limited feedback trials were used both in tests of retention and in the adaptation task. During these trials, the only visual feedback was a growing semicircular arc and a target arc placed 15 cm in front of the starting point. (G) Gaussian fits applied to “yes” responses of two representative participants, one who underwent cTBS stimulation to S1 and the other to M1.

Fig. 2.

Participants moved directly to the target point during baseline and compensated for the imposed visual perturbation during training. Movement direction was maintained in limited feedback trials. (A) Learning curves showing the average hand direction in all experimental conditions. SE are shown in shaded areas. Solid black lines show the ideal hand direction that would fully compensate for the imposed perturbation. (B) The mean hand direction during limited feedback trials. Error bars in (A and B) represent the mean and SE of the hand direction during baseline (Lower Left Corner) and plateau (Upper Right Corner).

Fig. 3.

MEPs were collected from the biceps brachii before and after cTBS stimulation to M1, S1, and control. The Individual MEPs are shown in dots with a straight line connecting the MEPs of each participant before and after the stimulation. Error bars represent the average and SE of each experimental condition. Statistical analysis indicated a significant decline in average MEP after cTBS stimulation to M1. No significant effect of cTBS on MEPs was found in the S1 and control conditions.

Fig. 4.

Following cTBS stimulation, memory for newly learned movements was assessed using either recognition or movement reproduction tests. (A) Average Gaussian fits to all yes/no responses during recognition tests. The direction corresponding to the Gaussian peak provides an estimate of remembered direction. It is seen that mean retention in the S1 condition is closer to zero than in the M1 and control conditions. Fits for M1 and control conditions overlap. (B) Binned recognition memory performance remained stable in all conditions throughout the test. To calculate each bin value, Gaussian curves were fitted to recognition judgments over a sliding window of 36 trials (Materials and Methods). The remembered direction in the S1 condition is reduced compared to that in the M1 and control conditions. (C) A direct comparison of remembered direction estimates, using Gaussian fits for individual participants in M1, S1, and control conditions. (D) Trial-to-trial hand movement direction during movement reproduction tests. The remembered direction for participants in the S1 condition was reliably less than that for participants in the M1 and control conditions. The average remembered direction for M1 and control conditions mostly overlaps. (E) The averaged binned data in D over a sliding window of 36 trials. (F) A direct comparison in remembered direction using the average of all trial-to-trial data points for each individual in the M1, S1, and control conditions. Statistical analysis indicated a significant drop in the remembered direction for S1 relative to M1 and control, indicating an adverse effect of S1 disruption on motor memory retention. In all panels, the mean values and SE are represented with solid lines and shaded areas, respectively.

Fig. 5.

To facilitate a comparison between recognition and movement reproduction tests, the same binning procedure was applied to each. (A) Estimates of the remembered direction in recognition tests are consistently closer to the learned direction than those in movement reproduction testing. (B) A direct comparison of recognition and movement reproduction scores for each participant following cTBS stimulation to each candidate brain area (M1, S1, and control). Statistical analysis found a significant difference in the remembered direction between recognition and movement reproduction tests in favor of recognition.

Fig. 6.

Additional control tests were conducted to verify that the impairment in remembered direction after cTBS stimulation to S1 was learning specific. Using both recognition and movement reproduction tests of retention, the remembered hand direction after a null rotated training task and cTBS to S1 was compared to remembered direction estimates previously acquired following visuomotor adaptation and cTBS to S1. (A) Gaussian estimates of the remembered direction in the unrotated S1 condition were close to zero indicating that cTBS does not affect movement direction in the absence of learning (B) Similar, near-zero estimates of remembered direction, were obtained using movement reproduction tests following null-rotation training and cTBS to S1. Once again, cTBS did not affect remembered movement direction in the absence of learning. (C) Binned data comparison shows that remembered direction estimates from recognition and reproduction tests mostly overlap for the unrotated S1 condition. (D) A direct comparison of remembered direction estimates in the S1 condition following visuomotor adaptation and following unrotated S1. In unrotated S1 conditions, no difference was found between the hand direction at the end of null-rotation training and during memory tests.