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Time-Varying Covariance of Neural Activities Recorded in Striatum and Frontal Cortex As Monkeys Perform Sequential-Saccade Tasks

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Time-Varying Covariance of Neural Activities Recorded in Striatum and Frontal Cortex As Monkeys Perform Sequential-Saccade Tasks Time-varying covariance of neural activities recorded in striatum and frontal cortex as monkeys perform sequential-saccade tasks N. Fujii*† and A. M. Graybiel*‡ *Department of Brain and Cognitive Sciences and the McGovern Institute for Brain Research, Massachusetts Institute of Technology, 45 Carleton Street, E25-618, Cambridge, MA 02139; and †Laboratory for Symbolic Cognitive Development, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan Contributed by A. M. Graybiel, May 2, 2005 Cortico-basal ganglia circuits are key parts of the brain’s habit circuit in macaque monkeys and simultaneously recorded neural system, but little is yet known about how these forebrain path- activity in these regions with multiple chronically implanted ways function as ingrained habits are performed. We simulta- electrodes as the monkeys viewed a sequence of visual targets neously recorded spike and local field potential (LFP) activity from and made saccades to each in order to receive reward. We regions of the frontal cortex and basal ganglia implicated in recorded from the oculomotor region of the caudate nucleus, the visuo-oculomotor control as highly trained macaque monkeys dorsolateral prefrontal cortex anterior to the frontal eye fields, performed sequences of visually guided saccades. The tasks were in which we have found saccade-related activity (10) and, in some repetitive, required no new learning, and could be performed experiments, the supplementary eye field (SEF) as well. To nearly automatically. Our findings demonstrate striking differ- achieve a population-level analysis, we recorded local field ences between the relative timing of striatal and cortical activity potential (LFP) activity (11–15) in addition to the spike activity during performance of the tasks. At the onset of the visual cues, of individual neurons. Our goal in these experiments was to LFPs in the prefrontal cortex and the oculomotor zone of the determine the patterns of activity that occur in these compart- striatum showed near-synchronous activation. During the period ments of oculomotor corticobasal ganglia circuits as the monkeys of sequential-saccade performance, however, peak LFP activity performed the sequential tasks in a stereotyped, habitual fash- occurred 100–300 msec later in the striatum than in the prefrontal ion. We therefore made the recordings after the monkeys had cortex. Peak prefrontal activity tended to be peri-saccadic, whereas been extensively trained on the saccade tasks, so that no new peak striatal activity tended to be post-saccadic. This temporal learning would be required of them. offset was also apparent in pairs of simultaneously recorded Our findings demonstrate that neural activity in each of the prefrontal and striatal neurons. In triple-site recordings, the LFP striatal and cortical regions was differentially modulated during activity recorded in the supplementary eye field shared temporal the course of task performance, but that, remarkably, the characteristics of both the prefrontal and the striatal patterns. The relative timing of peak neural activities in these regions varied near simultaneity of prefrontal and striatal peak responses at cue dynamically during the task. Cortical and striatal components of onsets, but temporal lag of striatal activity in the movement cortico-basal ganglia loops thus do not have a single timing periods, suggests that the striatum may integrate corollary dis- relationship during repetitive performance of familiar sequential charge or confirmatory response signals during sequential task tasks. Instead, both striatal and cortical levels appear to register performance. These timing relationships may be signatures of the sensory inputs at nearly the same time but have activities that normal functioning of striatal and frontal cortex during repetitive diverge in time during the execution phase of task performance. performance of learned behaviors. Materials and Methods basal ganglia ͉ local field potential ͉ prefrontal cortex ͉ synchrony Two adult female monkeys (Maccaca mulatta), M6 and M7, were trained over a period of 3 years to perform visuomotor tasks he basal ganglia and neocortex are strongly interconnected (10). For the main sequential-saccade task, the monkeys were Tby pathways that lead from widespread areas of the neocor- required to fixate for 1 sec on a red 0.8°-diameter target tex to the striatum and from the striatum through multisynaptic presented at the center of a 9 ϫ 9 array of gray potential target pathways back to the neocortex, mainly the frontal cortex (1). dots on a computer screen 30 cm in front of the monkey. The These cortico-basal ganglia loops are thought to release cortical fixation point was then extinguished, and the monkeys were activity phasically from tonic inhibitory control by the basal required to make saccades within 400 msec to one to six targets ganglia, thereby modulating cortical function (2, 3). Neuroim- successively illuminated in red (Go signals; estimated onset jitter, aging studies have demonstrated that cortical and striatal com- Ϸ14 msec). The lengths of the saccade sequences and target ponents of these forebrain circuits can be coactivated during presentation intervals were varied in blocks of 30–40 trials. The voluntary behavior, and that such coactivation patterns are monkeys received water reward 400–800 ms after the last target regionally selective (4, 5). Very little evidence is available, offset if they successfully completed a given saccade sequence in however, about how the temporal dynamics of ongoing activity a single trial. A 1.5-sec inter-trial interval followed. Target states in the basal ganglia and neocortex are interrelated as sequences for each trial were chosen pseudorandomly from 64 animals perform the habitual, semi-automatic behaviors that sequences for the standard four-target task, eliciting saccades in cortico-basal ganglia pathways are thought to enable. combinations of up, down, right, and left. Thus, in activity Resolving this issue is at the limits of current technology, averaged over successive trials, the effects of saccade direction because both population-level analysis across multiple brain were cancelled out. The monkeys were also trained on fixed- regions and high spatiotemporal resolution at a local level are required, together with large-scale identification of anatomically connected pairs of single neurons (6–9). As a step toward Abbreviations: SEF, supplementary eye field; LFP, local field potential. analyzing corticostriatal dynamics, we identified striatal and ‡To whom correspondence should be addressed. E-mail: [email protected]. cortical components of the oculomotor cortico-basal ganglia © 2005 by The National Academy of Sciences of the USA 9032–9037 ͉ PNAS ͉ June 21, 2005 ͉ vol. 102 ͉ no. 25 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0503541102 Downloaded by guest on October 2, 2021 sequence blocks of trials not reported here (10). The standard prefrontal cortex (n ϭ 52), and SEF (n ϭ 25) of the left number of saccades per trial was four, and the standard interval hemisphere. We applied a moving-window cross-covariance between the visual Go signals was 400 msec. In a variant of the analysis (MATLAB) to all pairs of simultaneously recorded LFPs standard task, on which monkeys were trained for Ͼ1.5 months to determine the temporal comodulation of LFP activity in the before recording, the color of the last target was yellow instead three structures. Two-hundred-msec-wide time windows were of red. A simple fixation task was also given, requiring 1-sec moved in steps of 100 msec across each pair of normalized fixation followed by reward 400–800 msec later. Trials with prefrontal-striatal, prefrontal-SEF, and SEF-striatal LFPs re- reward only, without reward but with reward-associated click, or corded over 60-trial blocks of the default four-saccade task. with clicks only were also given in blocks of 30 trials. Cross-correlograms were normalized by using the mean and A headpost, a recording chamber, and an eye coil (16) were standard deviation. We also applied the peak detection algo- surgically implanted in sterile surgeries performed by methods in rithm used above to the cross-correlation for each individual accordance with National Institutes of Health guidelines and time window to derive average peak and valley timing distribu- approved by the Massachusetts Institute of Technology Com- tion plots. mittee on Animal Care. Spike and LFP activities were recorded simultaneously from the caudate nucleus bilaterally and from the Results dorsolateral prefrontal cortex in the left hemisphere of each Task-Related Single-Unit Activity Recorded Simultaneously in Stria- monkey with 24–64 Epoxylite-coated tungsten microelectrodes tum and Prefrontal Cortex. We first analyzed neuronal activity in (FHC, Bowdoinham, ME; 0.2–1.5 mohm) advanced through paired simultaneous recordings of units at up to 21 sites in the supradural guide tubes in a grid. Up to 12 microelectrodes were dorsolateral prefrontal cortex and up to 20 sites in the caudate also placed in the left SEF in monkey M7. Electrode placement nucleus (Fig. 8, which is published as supporting information on was guided by pre-recording MRI images and by stimulation and the PNAS web site). The resulting sample of 750 well isolated recording mapping (10, 17). Electrodes were initially placed at units (n ϭ 156 in PFC, n ϭ 594 in caudate nucleus) included 90 sites with well-isolated unit activity, regardless of whether task- task-related neurons, of which 54
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