Neurons in Primary Motor Cortex Encode Hand Orientation in a Reach-to-Grasp Task

Abstract

It is disputed whether those neurons in the primary motor cortex (M1) that encode hand orientation constitute an independent channel for orientation control in reach-to-grasp behaviors. Here, we trained two monkeys to reach forward and grasp objects positioned in the frontal plane at different orientation angles, and simultaneously recorded the activity of M1 neurons. Among the 2235 neurons recorded in M1, we found that 18.7% had a high correlation exclusively with hand orientation, 15.9% with movement direction, and 29.5% with both movement direction and hand orientation. The distributions of neurons encoding hand orientation and those encoding movement direction were not uniform but coexisted in the same region. The trajectory of hand rotation was reproduced by the firing patterns of the orientation-related neurons independent of the hand reaching direction. These results suggest that hand orientation is an independent component for the control of reaching and grasping activity.

Keywords: Hand orientation; Non-human primate; Primary motor cortex; Single neuron recording.

Fig. 1

Experimental apparatus and sequence of events in the reach-to-grasp task. A The experimental apparatus included a central light, a central holding pad, two target lights, and two target objects at three orientations (45°, 90°, 135°). The target orientation definition is indicated. B The sequence of events and the trial epochs for the reach-to-grasp task in a typical successful trial. CHT center holding time, CRT cue reaction time, MT movement time, THT target holding time.

Fig. 2

Dependence of movement parameters on target orientation. A Averaged hand rotation trajectories (solid curves) ± SDs (dashed curves) during movements to targets oriented at 45° (red), 90° (blue), and 135° (black). Each solid curve was averaged from all trials of movements of monkey R to the same target fixed at the same orientation. Time zero is aligned on central pad release. B Averaged wrist transport velocity profiles to the same target at different orientations. Color index as in A. Time zero is also aligned on central pad release. The trajectory indicated that the reaching (transport) component was not influenced by the target orientation, but the hand orientation was modulated from movement initiation.

Fig. 3

Example of a motor cortical neuron encoding target orientation only. A Peri-event rasters and histograms during reach-to-grasp the target oriented at three different angles. Left column cell activity during movement to the left target; right column cell activity during movement to the right target. The three rows correspond to 45°, 90°, and 135° target orientations. Each raster illustrates the discharge pattern of the cell during 18 trials of movements to each target fixed at the same orientation. The rasters are ordered by trial sequence. Time zero is aligned on the central pad release (movement onset). Triangles target light on; diamonds target hit. The histograms were calculated with a bin-width of 20 ms. B Relationship between average firing rate and target orientation for this orientation-only neuron approximated by a linear regression.

Fig. 4

Example of a motor cortical neuron encoding target direction only. Peri-event rasters and histograms of a neuron encoding target direction only, as in Fig. 3A. Left column activity during movement to the left target; right column activity during movement to the right target.

Fig. 5

Example of a motor cortical neuron encoding both target orientation and movement direction. A Peri-event rasters and histograms of a neuron encoding both target orientation and movement direction, as in Fig. 3A, showing a positive correlation with hand orientation for both targets but significantly different average firing rates for the left and right targets. B Two significantly different positive linear relationships between firing rates and target orientations for the left and right targets of the neuron shown in (A).

Fig. 6

Example of a motor cortical neuron encoding an orientation-direction interaction. A Peri-event rasters and histograms of a neuron encoding an orientation-direction interaction, as in Fig. 3A. Shown is an opposite correlation between average firing rates and target orientations when reaching different target locations (negative for left target and positive for right target). B Positive and negative linear relationships exist between the firing rates and the target orientations during movement to the left and right targets for the neuron shown in (A).

Fig. 7

Distribution of 1676 task-related motor cortical neurons encoding target orientation and movement direction. A Pie chart showing the distribution of cortical encoding. B 3-D map of the 1676 task-related neurons. Each cross represents a single neuron; different colors indicate different orientation preferences: 45° (red), 90° (green), and 135° (blue). There was no clear topographic arrangement of neurons for different orientations as shown in (C, D): 141 orientation-only neurons from Monkey R and 172 from Monkey A.

Fig. 8

Density contours of orientation-only and direction-only cells. A, C Density contours of orientation-only cells in the chamber coordinates. B, D Direction-only cells in the chamber coordinates.

Fig. 9

Decoding error as a function of number of orientation-related motor cortical neurons and bin size. Sum of squared error calculated from the multiple linear regression results of 1–25 motor cortical neurons for the left (A) and right (B) targets. The four curves on each plot represent the bin sizes 50, 100, 150, and 200 ms.

Fig. 10

Reconstruction of hand orientation trajectories from motor cortical ensembles. A Hand orientation trajectories reconstructed using the multiple linear regression method. We used 50% of the data as training data, and the other 50% as the test data. Here, we only plotted the results from 15 trials for comparison with plot (B). Color index: 45° (black), 90° (blue), and 135° (purple); red dashed lines averaged actual hand orientation trajectories. B Hand orientation trajectories reconstructed using the artificial neural network method.