Behavioral context and coherent oscillations in the supplementary motor area

Abstract

Movements with similar physical characteristics can occur in various behavioral contexts, as when they are embedded in different sequences or when the expected outcomes of movements vary. Similarly, neurons in various sensory and motor structures in the brain commonly display modulations in their activity according to contextual factors, such as expected reward. Although these contextual signals must be combined with incoming sensory inputs to generate appropriate behaviors according to the animal's motivational state, the mechanisms by which these two signals are integrated remain poorly understood. The present study examined the effects of contextual factors on the magnitude of coherent oscillations in the activity of individual neurons recorded in the supplementary motor area (SMA) of monkeys during a serial reaction time task. In this task, the animal produced a predictable sequence of hand movements repeatedly according to visual instructions. The performance of the animal was influenced by the location of the rewarded target as well as the ordinal position of the movement. In contrast, the level of coherent oscillations in the activity of SMA neurons was affected only by the rewarded target location but not by the ordinal position of the movement sequence. In addition, changes in coherent oscillations were not accounted for by systematic changes in the mean firing rates. These results are consistent with the proposal that synchronous spikes might be used to control the flow of information and suggest that coherent oscillations in the SMA might encode contextual variables, such as expected reward.

Figure 1.

Spatial layout of the serial reaction time task with an example triplet of target locations indicated by gray disks. The target C (dark gray) corresponds to the rewarded location. Scale bar, 5 cm.

Figure 2.

Effects of rewarded target location and ordinal position of the movement on behavioral performance. The results for each of three movements in a triplet (A, B, C) are shown on the horizontal axis, and the three repetitions of the triplet are shown by white, gray, and black disks (numbered 1, 2, and 3, respectively). Error bars, corresponding to 2× SEM, are shown only when the SEM is larger than the size of the symbol.

Figure 3.

Phase-locking index computed separately for nine movements in each trial (A1 through C3). Phase-locking index computed for the first, second, and third repetition of the triplet is shown on the rightmost column (labled 1, 2, 3), and the results for each of the three movements in the triplet are shown at the bottom (labeled A, B, C).

Figure 4.

Top row, Average phase-locking index during the last 200 msec of the hold period plotted as a function of the frequency of coherent oscillation. Middle row, Average phase-locking index during the same period computed from the gamma surrogate spike trains (Lee, 2003). Vertical lines in the middle and right columns correspond to the frequency of 32.5 Hz used for a regression analysis. Bottom row, Population-averaged spike density functions. The results are shown separately for individual movements (left), for three movements in the triplet (middle column), and for three cycles of the triplet (right).