Spatial and temporal eye-hand coordination relies on the parietal reach region

Abstract

Coordinated eye movements are crucial for precision control of our hands. A commonly believed neural mechanism underlying eye-hand coordination is interaction between the neural networks controlling each effector, exchanging, and matching information, such as movement target location and onset time. Alternatively, eye-hand coordination may result simply from common inputs to independent eye and hand control pathways. Thus far, it remains unknown whether and where either of these two possible mechanisms exists. A candidate location for the former mechanism, interpathway communication, includes the posterior parietal cortex (PPC) where distinct effector-specific areas reside. If the PPC were within the network for eye-hand coordination, perturbing it would affect both eye and hand movements that are concurrently planned. In contrast, if eye-hand coordination arises solely from common inputs, perturbing one effector pathway, e.g., the parietal reach region (PRR), would not affect the other effector. To test these hypotheses, we inactivated part of PRR in the macaque, located in the medial bank of the intraparietal sulcus encompassing the medial intraparietal area and area 5V. When each effector moved alone, PRR inactivation shortened reach but not saccade amplitudes, compatible with the known reach-selective activity of PRR. However, when both effectors moved concurrently, PRR inactivation shortened both reach and saccade amplitudes, and decoupled their reaction times. Therefore, consistent with the interpathway communication hypothesis, we propose that the planning of concurrent eye and hand movements causes the spatial information in PRR to influence the otherwise independent eye control pathways, and that their temporal coupling requires an intact PRR.

Keywords: PPC; inactivation; movement endpoints; reaches; reaction time; saccades.

Figure 1.

Natural eye–hand coordination in the eye–hand task. a, The temporal sequence of events in the eye–hand task. Eyes were unconstrained. b, The inactivation site shown on the horizontal brain MRI slice. The bright spot indicates where MR visible gadolinium was injected in the same way as muscimol. c, The hand and eye positions of seven example trials in the eye–hand task are aligned to the go cue. Each pair of a solid and a dashed line in the same color represents the hand and eye positions of the same single trial. The arrows mark the positions of the central hand-fixation and the reach target. d, Reach and saccade endpoints for six target locations in the eye–hand task from an example pair of a control and an inactivation session. The saccades occurred under free-gaze condition in the absence of experimental requirements.

Figure 2.

PRR inactivation shortens the amplitude of coordinated saccades and reaches but not of saccades executed alone. a, Reach and saccade amplitudes in three task conditions for each of six target locations. For each target, the mean amplitude and its 95% confidence interval are plotted for control versus inactivation reaches in the eye–hand task, control versus inactivation saccades in the eye–hand task, control versus inactivation reaches in the hand-only task, and control versus inactivation saccades in the saccade-only task, from left to right. The horizontal dashed line in each plot marks the target amplitude. b, Within-session means of reach and saccade amplitudes in the eye–hand task for the contralateral target, in control versus inactivation sessions. Each pair of a control and an inactivation session is connected with a solid line if their means are significantly different (p < 0.05), and with a dashed line otherwise.

Figure 3.

PRR inactivation weakens the temporal correlation between spatially coordinated reaches and saccades. a, Saccade reaction times versus reach reaction times (RTs) for the contralateral target in the eye–hand task for all control versus inactivation trials. Each dot represents a single trial, and the lines are the linear regression. b, The mean and its 95% confidence interval of the correlation coefficient between saccade and reach RTs of all control versus inactivation trials for each of the six target locations. c, Within-session RT correlation coefficients for the contralateral target, in control versus inactivation sessions. Each pair of a control and an inactivation session is connected with a solid line if their coefficients are significantly different (p < 0.05), and with a dashed line otherwise.