Neuroscience Letters, 111 (1990) 151-156

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Elsevier Scientific Publishers Ireland Ltd. NSL 06730

A comparison of preparation-related neuronal activity changes in the prefrontal, premotor, primary motor and posterior parietal areas of the monkey cortex: preliminary results Jean Requin, Jean-Claude Lecas* and Nicole Vitton Unit of Cognitive Neurosciences, Laboratory of FunctionalNeurosciences, National Centerfor Scientific Research, Marseilles (France)

(Received 10 February 1989; Revised version received 17 November 1989;Accepted 24 November 1989) Key words: Motor activity; Motor preparation; Prefrontal cortex; Primary motor cortex; Premotor cor-

tex; Posterior parietal cortex Single-unit activity of prefrontal (PF), premotor (PM), primary motor (MI) and posterior parietal (PP) cortical areas was analysed from 3 monkeys trained to perform visually guided ann movements in a between-arms choice reaction time (RT) task. Percentages of preparation-related units, i.e. units whose change in activity during the preparatory period was correlated with RT, were 19% in PF, 31% in MI, 46 % in PM and 68 % in PP, respectively. These data support the hypothesis that neural pathways connecting PP association areas to MI, via PM, are involved mainly in movement planning. In a previous study [3], we analysed the changes in neuronal activity o f the m o n k e y primary m o t o r (MI) cortex during preparation for movement. M o n k e y s were trained to perform a between-arms choice reaction time (RT) task after a 1 s preparatory period. The degree o f preparation for performing m o v e m e n t o f either forearm was changed by manipulating the relative probabilities for the left and right arms to perform the movement. This manipulation resulted in a decrease in R T as response probability increased, while m o v e m e n t time (MT) was not affected. Single-cell recording techniques were used to study the neuronal activity o f M I during task performance. A m o n g 1 19 units whose activity was recorded during an experimental session, statistically significant trial-by-trial correlations between intra-session changes in unit activity during the p r e p a r a t o r y period and R T were found in 31% o f units when contralateral m o v e m e n t s as well as when ipsilateral movements were considered. With the same experimental procedure, we had the o p p o r t u n i t y to record - either simultaneously with M I recordings or not - in different cortical areas including: (1) *Present address: LPN/CNRS, 91190 Gif-sur-Yvette, France. Correspondence: J. Requin, C.N.R.S.-LNF 1, 31, Chemin Joseph-Aiguier, 13402 Marseille Cedex 9, France. 0304-3940/90/$ 03.50 © 1990 Elsevier Scientific Publishers Ireland Ltd.

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prefrontal (PF) cortex around the principal sulcus, (2) premotor cortex (PM) rostrally to the arcuate sulcus, i.e. in area 6, (3) posterior parietal (PP) cortex around the intraparietat sulcus, i.e. in areas 5 and 7. The data so collected, together with those previously found by studying MI, made it possible to compare the preparationrelated activity in different cortical areas which have been proposed, in different ways, to be involved in movement control processes. Bearing in mind our criterion for defining preparatory neuronal activity i.e., predictive value for RT performance it was of special interest (a) to confirm data showing that set-related neuronal activity [11] as well as directionally selective preparation activity [7] were found more often in PM than in MI, and, (b) to know the part played in preparatory processes by association cortical areas, especially PP which has sometimes been viewed as the primum movens in movement planning [4, 8]. Methods used in this study have been extensively described elsewhere [3]. Three monkeys, one left-handed and two right-handed, were trained to press upon two levers with both hands and, after a preparatory period of 1 s duration initiated by a warning signal, to point as quickly as possible at either a left- or right-located target, when illuminated as a response signal, with either the left or right hand. This pointing movement was performed mainly by a flexion of the forearm, as confirmed, on electromyographic recordings, by a clear-cut activation of the biceps. During an experimental session, the probability that each target would be illuminated was varied by blocks of 64 trials, presented in a random order, from 0 to 1.00 in steps of 0.25. After training, usual surgical procedures were used to make a craniotomy on the side contralateral to the best performing arm according to RT data. A rectangular chamber was then adapted over the skull opening, making possible the penetration of tungsten epoxy-varnished microelectrodes transdurally into the cortex. The size of the skull section (41 mm length × 10.5 mm wide) enabled (a) the recording of neuronal activity from the principal sulcus rostrally to the lunate sulcus caudally and (b) to use occasionally two micromanipulators in order to record simultaneously in two different cortical areas. In some sessions, neuronal activity was thus recorded in MI and either in PF or in PP, while in some other sessions neuronal activity was recorded in PM and PP. After being amplified, neuronal activity together with RT, i.e. the time between the target illumination and lever release, were analysed in two ways. First, displays either in raster or in histograms form, that were time-locked either to the warning signal or to the lever release, were made. Second, trial-by-trial correlations (by computing Bravais-Pearson's r) between the RT and spike frequency during the preparatory period were made for each unit. At the end of the experiment, monkeys were killed for histological examination and anatomical localization of electrode penetrations. The anatomical location of electrode penetrations in the 4 areas investigated is shown in Fig. 1. Locations of units which exhibited a preparation-related activity, i.e. changes in activity during the preparatory period were correlated with RT, and which did not exhibit such an activity, are shown. Number and percentage (of total

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Fig. 1. Anatomical location of electrode penetrations shown on a generalized representation of the cortical surface of the different hemispheres. Locations of units which exhibited preparation-related changes in activity are indicated by black circles.

number of units recorded) of preparation-related units found in the different areas are presented in Table I. They were classified according to the type of movementrelated activity that the units exhibited: a unit could be either excited, inhibited or unresponsive during movement performance. Moreover a unit could be activated either during the pointing movement performed by the arm either contralateral or ipsilateral to the recording site, or during movements of either arm. Percentages of units exhibiting a preparation-related activity were 19 % in PF, 31% in MI, 46% in PM and 68 % in PP, respectively. An overall comparison of these percentages shows that they statistically differ 0f2= 13.05, P < 0.01). However, pair-comparisons (cf. Table I) show that the difference in the number of preparation-related units is significant between PP and PF (Z2= 10.92, P!i ,i:~-~ ¸

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Fig. 2. Changes in activity of 2 units recorded in PF (top), 2 units recorded in PM (middle) and 2 units recorded in PP (bottom), Neuronal activity, either in the form of raster displays or histograms (20 ms bin width), are shown for movements performed by either the right or the left arm, either contralateral or ipsilateral to the recording site (see text). In the left part of the figure, neuronal activity is time-locked

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0(2= 5.38, P < 0.05), and between PP and M I (,~2= 7.16, P < 0.01), but does not reach statistical significance between PF and MI (;(2= 2.12, P > 0.10), between PM and PP 0(2= 1.28, P>0.10) and between PM and MI (3(2=2.08, P > 0.10). Examples of units exhibiting a preparation-related activity are presented in Fig. 2. No example of such a unit in MI was presented, since a detailed analysis of data collected in this area can be found in Lecas et al. [3]. On the top of Fig. 2, the changes in activity of two units (66 and 196) recorded in PF are shown. Unit 66, which was recorded on the left-handed monkey, was slightly excited during the preparatory period and then during the movement performed by the arm ipsilateral to the recording site. Changes in discharge frequency during the preparatory period were negatively correlated with RTs ( r = - 0 . 4 6 ; P

A comparison of preparation-related neuronal activity changes in the prefrontal, premotor, primary motor and posterior parietal areas of the monkey cortex: preliminary results.

Single-unit activity of prefrontal (PF), premotor (PM), primary motor (MI) and posterior parietal (PP) cortical areas was analysed from 3 monkeys trai...
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