TEMPORAL ENCODING OF MOVEMENT KINEMATICS IN THE DISCHARGE OF PRIMATE PRIMARY MOTOR AND PREMOTOR NEURONS

Citation
Qg. Fu et al., TEMPORAL ENCODING OF MOVEMENT KINEMATICS IN THE DISCHARGE OF PRIMATE PRIMARY MOTOR AND PREMOTOR NEURONS, Journal of neurophysiology, 73(2), 1995, pp. 836-854
Citations number
72
Categorie Soggetti
Neurosciences,Physiology,Neurosciences,Physiology
Journal title
ISSN journal
00223077
Volume
73
Issue
2
Year of publication
1995
Pages
836 - 854
Database
ISI
SICI code
0022-3077(1995)73:2<836:TEOMKI>2.0.ZU;2-H
Abstract
1. Several neurophysiological studies of the primary motor and premoto r cortices have shown that the movement parameters direction, distance , and target position are correlated with the discharge of single neur ons. Here we investigate whether the correlations with these parameter s 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 stu dy of neuronal specification of movement parameters. We recorded the a ctivity of single neurons in the primary motor and premotor cortices o f two rhesus monkeys (Macaca mulatta) while the animals performed reac hing movements made in a horizontal plane. Specifically, the animals m oved from a centrally located start position to 1 of 48 targets (1 cm( 2)) placed at eight different directions (0-360 degrees in 45 degrees intervals) and six distances (1.4-5.4 cm in 0.8-cm increments) from th e start position. 3. We analyzed 130 task-related cella of these, 127 (99 in primary motor cortex, 28 near the superior precentral sulcus) h ad average discharges that were significantly modulated with the movem ent and were related to movement direction, distance, or target positi on. To determine the temporal profile of the correlation of each cell' s discharge with the three parameters, we performed a regression analy sis of the neural discharge. We calculated partial R(2)s for each para meter and the total R(2) for the model as a function of time. 4. The d ischarge 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 and ordering in t he onset of the parameter-related partial R(2) values: direction-relat ed discharge occurred first (115 ms before movement onset), followed s equentially by target position (57 ms after movement onset) and moveme nt 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 R(2) curves (4 8, 254, and 515 ms after movement onset, respectively, for direction, target position, and distance). The partial R(2) profile for direction had a higher peak value but a shorter duration than that for both tar get 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. F or some cells that were related to two or more parameters, the partial R(2)s waxed and waned in a reciprocal manner during the transition pe riod. A high partial R(2) for one parameter at a given moment in time was often associated with a low partial R(2) 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 duri ng these transition periods. During the transition period from directi on to target position, a large number of cells had a low index of simu ltaneity, indicating that the discharge of these cells is correlated w ith only one parameter at a time. 7. The timing differences in the par ameter-related discharge of motor and premotor neurons have three impl ications. First, these parameters are processed serially. Second becau se each parameter has a relatively distinct time course, the correlati ons with direction, X-Y-position of the target and movement distance e xhibit 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 res ults demonstrate that single cells can encode multiple parameters by a temporal parcellation scheme. This scheme avoids the ambiguities of f iring rate simultaneously encoding more than one parameter.