Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons

Q. G. Fu, D. Flament, J. D. Coltz, T. J. Ebner

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234 Scopus citations

Abstract

1. Several neurophysiological studies of the primary motor and premotor cortices have shown that the movement parameters direction, distance, and target position are correlated with the discharge of single neurons. Here we investigate whether the correlations with these parameters occur simultaneously (i.e., parallel processing), or sequentially (i.e., serial processing). 2. The single-unit data used for the analyses presented in this paper are the same as those used in our earlier study of neuronal specification of movement parameters. We recorded the activity of single neurons in the primary motor and premotor cortices of two rhesus monkeys (Macaca mulatta) while the animals performed reaching movements made in a horizontal plane. Specifically, the animals moved from a centrally located start position to 1 of 48 targets (1 cm2) placed at eight different directions (0-360° in 45° intervals) and six distances (1.4-5.4 cm in 0.8- cm increments) from the start position. 3. We analyzed 130 task-related cells; of these, 127 (99 in primary motor cortex, 28 near the superior precentral sulcus) had average discharges that were significantly modulated with the movement and were related to movement direction, distance, or target position. To determine the temporal profile of the correlation of each cell's discharge with the three parameters, we performed a regression analysis of the neural discharge. We calculated partial R2s for each parameter and the total R2 for the model as a function of time. 4. The discharge of the majority of units (73.2%) was significantly correlated for some time with all three parameters. Other units were found that correlated with different combinations of pairs of parameters (21.3%), and a small number of units appeared to code for only one parameter (5.5%). There was no obvious difference in the presence of correlations between cells recorded in the primary motor versus premotor cortices. 5. On average we found a clear temporal segregation anti ordering in the onset of the parameter-related partial R2 values: direction-related discharge occurred first (115 ms before movement onset), followed sequentially by target position (57 ms after movement onset) and movement distance (248 ms after movement onset). Some overlap in the timing of the correlation of these parameters was evident. We found a similar sequential ordering for the latency of the peak of the R2 curves (48,254, and 515 ms after movement onset, respectively, for direction, target position, and distance). The partial R2 profile for direction had a higher peak value but a shorter duration than that for both target location and distance. An additional set of univariate regression analyses demonstrated that the sequential ordering of the correlations was preserved, with direction occurring first and distance last. 6. For some cells that were related to two or more parameters, the partial R2s waxed and waned in a reciprocal manner during the transition period. A high partial R2 for one parameter at a given moment in time was often associated with a low partial R2 for the other parameter. We developed an index of simultaneity and measured the degree to which cell firing was correlated significantly with the two parameters during these transition periods. During the transition period from direction to target position, a large number of cells had a low index of simultaneity, indicating that the discharge of these cells is correlated with only one parameter at a time. 7. The timing differences in the parameter-related discharge of motor and premotor neurons have three implications. First, these parameters are processed serially. Second, because each parameter has a relatively distinct time course, the correlations with direction, X-Y position of the target, and movement distance exhibit considerable independence. Third, the observation that distance modulation mostly occurs after the time of peak velocity suggests that the distance coding does not specify the movement velocity. These results demonstrate that single cells can encode multiple parameters by a temporal parcellation scheme. This scheme avoids the ambiguities of firing rate simultaneously encoding more than one parameter.

Original languageEnglish (US)
Pages (from-to)836-854
Number of pages19
JournalJournal of neurophysiology
Volume73
Issue number2
DOIs
StatePublished - 1995

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