Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze–reach movements

Abstract

One must be quick and precise when foveating targets to be reached, because the eyes have to guide the hand trajectory by visual feedback, and we may miss a rapidly moving target if our grasping is not fast and accurate enough. To this end, our brains developed mechanisms coordinating gaze and hand movements to optimize the way in which we foveate and reach. One of these mechanisms is the facilitation of the primary saccade--proven in humans and confirmed here in monkeys--which allows the generation of short-latency gaze movements when reaching towards visual targets. Here we tested whether the neuronal activity in the superior colliculus (SC) accounts for this mechanism; alternatively, cortical saccade-related areas could play a major role in the fast initiation of saccades during such elaborated behaviours bypassing the SC. Upon presentation of a target, neurons located at the rostral pole of the SC started the saccade-related pause in their activity earlier in tasks involving coordinated gaze-reach movements than in tasks in which the saccades were made in isolation. In the same tasks neurons located at the caudal SC reached peak firing rates earlier in coordinated gaze-reach movements than with isolated saccades, confirming the tight coupling between their burst activity latencies and the saccadic reaction times. In sum, our results extend the role of the SC in saccade initiation to coordinated gaze-reach movements, identifying its activity as an important part of the distributed neural system for eye-hand coordination.

Arm Movements Induced by Electrical Microstimulation in the Superior Colliculus of the Macaque Monkey

“…Although this confound cannot be ruled out in any experiment using electrical microstimulation in interconnected neural networks, we think it is not very likely for the following reasons. First, our thresholds to elicit arm movements (median 30 A) are well below mean currents necessary to antidromically activate corticotectal axons (182, 200, or 25-1800 A for axons from LIP, FEF, or premotor cortex, respectively (Paré and Wurtz, 1997;Sommer and Wurtz, 2000;Reyes-Puerta and Hoffmann, 2010). Thresholds for orthodromic spikes in FEF or premotor cortex driven from SC are in a similar range (Sommer and Wurtz, 1998;Reyes-Puerta and Hoffmann, 2010).…”

“…First, our thresholds to elicit arm movements (median 30 A) are well below mean currents necessary to antidromically activate corticotectal axons (182, 200, or 25-1800 A for axons from LIP, FEF, or premotor cortex, respectively (Paré and Wurtz, 1997;Sommer and Wurtz, 2000;Reyes-Puerta and Hoffmann, 2010). Thresholds for orthodromic spikes in FEF or premotor cortex driven from SC are in a similar range (Sommer and Wurtz, 1998;Reyes-Puerta and Hoffmann, 2010). Second, according to Phillips (1959), Betz-cells in the cat's motor cortex show an early fascilitation followed by long-lasting depressed excitability after stimulation of pyramidal tract axons.…”

“…All experiments were approved by the local ethics committee and performed in accordance with the Deutsche Tierschutzgesetz of 7-26-2002, the European Communities Council Directive of 86 609 EEC, and the NIH Guide for the Care and Use of Laboratory Animals. Subjects M1 and M3 also participated in related experiments (Reyes-Puerta et al, 2009.…”

Timing and communication of parietal cortex for visuomotor control

“…The final temporal locking between eye and hand information could be achieved in the superior colliculus (SC), which in addition to the projections from IPL and FEF, is also target of projections from the 'lateral grasping network' [48 ]. If similar projections also arise from the SPL areas, as it is reasonable to assume by the presence of reach-related neurons in the SC [49], a combined cortical input from both SPL and IPL could temporally lock eye and hand movement, thus shaping the temporal activation profile of reach neurons in the SC and underlying reticular formation [49]. At the motor output level, cortico-spinal and reticulo-spinal projections on spinal interneurons will convey hand information already temporally locked to the eye, also thanks to the projection from SC to the saccade generators of the midbrain and pons.…”

Response Inhibition

“…Although the SC has for decades been implicated in eye movement control, recent studies have suggested its role in arm and hand movement control in monkeys (Philipp & Hoffmann, 2014) and humans (Himmelbach et al, 2013). The neuronal responses in SC can be tied to gaze shift for eye-hand coordination (Reyes-Puerta et al, 2011). Inactivation of the SC causes target selection deficits for reaching movements that cannot be accounted for by impairment in visual perception or motor execution (Song et al, 2011).…”