Local field potentials in the parietal reach region reveal mechanisms of bimanual coordination

Abstract

Primates use their arms in complex ways that frequently require coordination between the two arms. Yet the planning of bimanual movements has not been well-studied. We recorded spikes and local field potentials (LFP) from the parietal reach region (PRR) in both hemispheres simultaneously while monkeys planned and executed unimanual and bimanual reaches. From analyses of interhemispheric LFP-LFP and spike-LFP coherence, we found that task-specific information is shared across hemispheres in a frequency-specific manner. This shared information could arise from common input or from direct communication. The population average unit activity in PRR, representing PRR output, encodes only planned contralateral arm movements while beta-band LFP power, a putative PRR input, reflects the pattern of planned bimanual movement. A parsimonious interpretation of these data is that PRR integrates information about the movement of the left and right limbs, perhaps in service of bimanual coordination.

Fig. 1. Delayed movement tasks and recording sites.

a On each trial, after an initial fixation, a peripheral target appeared and instructed the spatial location and effector to be used (eyes or arm[s]) for the subsequent movement(s). The stimulus remained visible during a variable delay period. Throughout saccade and unimanual reach trials, the hand(s) that were not instructed to move were required to remain on the home pad(s). After the go cue (fixation offset), animals made the instructed movements to the target location(s). On single-target trials, eye movements to the target were required. Movements were either into or 180 degrees out of the RF. On bimanual-apart reach trials, eye movements were unconstrained once the animals were cued to initiate the movement. One arm moved into the RF and the other arm moved out of the RF on each trial. Movement directions and movement types were randomly interleaved. A saccade-only trial (white stimulus) is depicted. b Unimanual left or right arm reaches were instructed with a single green or red peripheral target, respectively. Reaches with both arms to a single target (bimanual-together) were instructed with a blue stimulus. Reaches with each arm to a different target (bimanual-apart) were instructed with one red and one green stimulus separated by 180 degrees across the central fixation. Unimanual reaches were either to targets on the same side of the body (upper row) or crossed to the opposite side of the body (lower row). Bimanual-apart reaches were made with the arms either uncrossed (upper row) and or crossed (lower row). Note that only one of the 4 possible target pairs is illustrated. c Recording sites from the right hemisphere of each monkey. Coordinates of recorded cells in MkT (upper row) and MkZ (lower row) are shown projected to a single MRI section perpendicular to the path of the recording electrode, with zoomed-in views on the right. IPS, intraparietal sulcus; Midline, longitudinal fissure; POS, parieto-occipital sulcus; STS, superior temporal sulcus. The colored regions are from; LIP, lateral intraparietal area; LOP, lateral occipital-parietal area; MIP, medial intraparietal area; PO, parietal-occipital area. The medial, lateral, anterior, and posterior directions are labeled as M, L, A, and P, respectively. The size of each circle indicates the number of cells recorded along that track. LFP recordings were obtained at these locations and other sites within 2 mm. Left hemisphere sites (not shown) are similar.

Fig. 2. Beta-band LFP–LFP coherence between PRR in the left and right hemispheres distinguishes bimanual-together and bimanual-apart movements from baseline and from unimanual movements.

Coherence in the beta band (~20–30 Hz) is elevated for bimanual-together movements (blue) and decreased for bimanual-apart movements (purple) compared to unimanual reaches (yellow) or to the baseline period (gray). Coherence during saccade trials (black) resembled that seen during unimanual reach. Data are averaged from the 113 pairs of sites (43 from MkT, 70 from MkZ) recorded simultaneously in the two hemispheres, with coherence measured in the −500–0 ms interval before the cue to move. Blue and purple asterisks indicate significant differences of bimanual-together and bimanual-apart, respectively, versus unimanual. Gold asterisks denote comparison of bimanual-together versus bimanual-apart (two-sided t-tests, large asterisks = P < 0.05 after Bonferroni correction for testing at each of the 39 different frequency values plotted in the figure). Coherence outside the pictured range (from 16 to 20 Hz and 100 to 240 Hz) was unaffected (corrected P > 0.05). Error bars = ±1 s.e.m. Source data are provided as a Source Data file.

Fig. 3. A comparison of neural activity during 5 movement conditions.

Data on the left are aligned to target onset (solid vertical line) and truncated at the time of the earliest cue to initiate movement. Data on the right show the mean activity for preferred direction movements, relative to baseline, in the interval from 650 to 1150 ms (gray rectangle). a Beta-band LFP power (20–30 Hz) contains information about movement type. Power is computed in ±200 ms intervals every 100 ms. Colored shading indicates ±1 s.e.m. Responses to preferred and null directions showed no difference and so are merged across n = 312 sites. b Gamma-band LFP power (70–120 Hz) is similar but not identical to unit activity and unlike the beta band contains little additional information. (See text for additional detail.) Format as in a except that preferred and null directions are shown separately. Power is computed in ±100 ms intervals every 50 ms. c Single-unit activity is high when the animal prepares a contramanual reach in the preferred direction, whether alone (contramanual, solid red line), with an ipsimanual reach in the same direction (bimanual-together, blue), or with an ipsimanual reach in the opposite direction (bimanual-apart, purple). Firing is intermediate for preferred direction saccades and for preferred direction ipsimanual reaches (solid green and black), and for bimanual reaches in which the ipsilateral arm moves in the preferred direction and the contralateral arm moves out (bimanual-apart, dashed purple). (Bimanual-apart reaches are labeled based on the direction of the contralateral arm.) Activity is low for single-target movements in the null direction (dashed lines) during the delay period, independent of the movement type. Note that the divergence of firing rate associated with movement type (dotted vertical line) occurs ~100 ms sooner than the divergence in beta LFP power associated with movement type. Data from n = 113 single units. Colored shading indicates ±1 s.e.m. Source data are provided as a Source Data file.

Fig. 4. LFP power as a function of movement type and frequency.

LFP power is computed over the delay period for movements in the preferred and null directions. In the 16–32 Hz range power depends on task and frequency. In the 70–170 Hz range power depends on the task and is relatively stable across frequency. Data are for the 113 sites from which a tuned unit was simultaneously obtained. Source data are provided as a Source Data file.

Fig. 5. Interhemispheric beta-band spike-LFP coherence distinguishes between bimanual-together and bimanual-apart movements.

a Schematic model depicting local and distal inputs and outputs to and from PRR. Mass input and output of PRR is shown as arrows. The axon terminals of most neurons contact other neurons locally (light gray arrows), but some portion project distally, including to the homotopic area in the opposite hemisphere (dark gray arrows). Connections with non-homotopic areas are omitted for clarity. b Identical spike-LFP coherence predictions under interhemispheric communication scenario (black curve) and common input scenario (gray curve). c From 20 to 50 Hz, spike-LFP coherence is consistently high for bimanual-together movements (solid blue), intermediate for unimanual movements (solid green), and low for bimanual-apart movements (solid purple). The distributions of coherence expected by chance were computed by shuffling interspike intervals. The medians of these distributions are shown as dashed traces. The gray shaded region covers 95% of the values expected by chance; values that exceed this are marked by thickened lines (P < 0.05). Values exceeding the light gray line are significant at P < 0.01. Note that there is no effect of movement type on the shuffled coherences. For this reason, data are pooled across movement types for the P < 0.05 and P < 0.01 thresholds. Coherences that are significantly larger for bimanual-together compared to bimanual-apart are indicated by asterisks (two-tailed t-test, P < 0.05). Dashed vertical lines indicate the beta range (20–30 Hz). Coherence was measured during the 800 ms before the go cue. Data are averaged from n = 42 pairs of sites (24 from MkT, 18 from MkZ) recorded simultaneously in the two hemispheres. Only sites with at least 500 spikes are shown. d Schematic model depicting common input to PRR in each hemisphere. Spike-LFP coherence predictions for common input model. e Lagged spike-LFP coherence predictions for direct communication and common input models, respectively. f Extremes of spike-LFP coherence (24–38 Hz) occur when spikes lead LFP by 10–15 ms (gray lines). Positive and negative x axis values indicate the relative temporal relationship between spike times and the LFP in the original data. Source data are provided as a Source Data file.