Heterogeneous neural coding of corrective movements in motor cortex

Abstract

During a reach, neural activity recorded from motor cortex is typically thought to linearly encode the observed movement. However, it has also been reported that during a double-step reaching paradigm, neural coding of the original movement is replaced by that of the corrective movement. Here, we use neural data recorded from multi-electrode arrays implanted in the motor and premotor cortices of rhesus macaques to directly compare these two hypotheses. We show that while a majority of neurons display linear encoding of movement during a double-step, a minority display a dramatic drop in firing rate that is predicted by the replacement hypothesis. Neural activity in the subpopulation showing replacement is more likely to lag the observed movement, and may therefore be involved in the monitoring of the sensory consequences of a motor command.

Keywords: double-step; motor cortex; neural coding; reaching; target jump.

FIGURE 1

Schematic of the two hypotheses for neural coding during a double-step. (A) Top: The theoretical double-peaked velocity profile of a double-step trial (black) can be decomposed into the sum of a primary velocity profile (light gray) and an overlapping, secondary velocity profile (dark gray); middle: Under the default “Summed” hypothesis, neural firing is predicted to track the observed velocity profile, preceding it at a fixed lead; bottom: The alternative “Replaced” hypothesis predicts that the neural firing will track the primary velocity profile (light gray), before replacing this with coding of the secondary profile (dark gray). (B) The predictions under the “Summed” and “Replaced” hypotheses if neuronal firing instead lags the observed velocity. The replacement between coding of the primary and secondary movements is assumed to happen at a fixed delay that we call the neural offset, prior to the start of the second movement (dashed line).

FIGURE 2

Location of the five multi-electrode arrays relative to the central sulcus (CS) and the arcuate sulcus (AS). (A) Subject CO had arrays in primary motor cortex (MI), dorsal premotor cortex (PMd), and ventral premotor cortex (PMv). (B) Subject MK had one array in MI. (C) Subject BO had one array in PMd.

FIGURE 3

Decomposition of actual kinematics observed during a double-step. (A) The actual kinematics of a double-step trail (black line) are well-approximated by the sum (gray line) of a primary (light gray) and secondary (dark gray) single-peaked profiles. (B) The single-trial velocity profiles are displayed as heat maps, with the vertical axis representing different trials, and the horizontal axis representing time elapsed within a given trial. The actual kinematics (top left) can be compared to the fit kinematics (top right), which is the sum of the single-trial primary (bottom left) and secondary (bottom right) motions.

FIGURE 4

The distribution of neural offsets is compared between neurons from the primary motor cortex (A) and the premotor cortex (B), including both dorsal and ventral premotor cortices. The neural offset describes the time at which the “Replaced” hypothesis predicts a shift from coding the primary movement to coding the secondary movement (see Figure 1).

FIGURE 5

A neuron from ventral premotor cortex is better fit by the “Summed” hypothesis. (A) During single-step (SS) trials, the observed peri-event time histogram (PETH, black) is well fit by a model assuming linear encoding of velocity and speed (gray dot dash). Zero time refers to the time of target appearance. (B) During double-step (DS) trials, the observed PETH (black) is well fit by the “Summed” prediction (gray dotted) but not the “Replaced” prediction (gray dashed). Zero time refers to the time of the target jump. (C) The single-trial spike time rasters for the SS trials. (D) The single-trial spike time rasters for the DS trials, arranged by the predicted replacement time (gray). (E) The DS single-trial prediction of the “Summed” hypothesis, displayed as a heat map. (F) The DS single-trial prediction of the “Replaced” hypothesis.

FIGURE 6

A neuron from ventral premotor cortex is better fit by the “Replaced” hypothesis. Format follows Figure 5.

FIGURE 7

A neuron from primary motor cortex is better fit by the “Replaced” hypothesis. Format follows Figure 5.

FIGURE 8

A neuron from dorsal premotor cortex is better fit by the “Replaced” hypothesis. Format follows Figure 5.

FIGURE 9

The distribution of the encoding time delay δ is compared between neurons which were better fit with the “Replaced” hypothesis (A), versus neurons better fit with the “Summed” hypothesis (B). Only neurons which showed a significant difference in single-trial root-mean-square error between the two hypotheses are shown (see Results for details).