Representation of Horizontal Head-on-Body Position in the Primate Superior Colliculus

Abstract

Movement-related activity within the superior colliculus (SC) represents the desired displacement of an impending gaze shift. This representation must ultimately be transformed into position-based reference frames appropriate for coordinated eye-head gaze shifts. Parietal areas that project to the SC are modulated by the initial position of both the eye-re-head and head-re-body and SC activity is modulated by eye-re-head position. These considerations led us to investigate whether SC activity is modulated by the head-re-body position. We recorded activity from movement-related SC neurons while head-restrained monkeys performed a delayed-saccade task. Across blocks of trials, the horizontal position of the body was rotated under a space-fixed head to three to five different positions spanning +/-25 degrees . We observed a significant influence of body-under-head position on SC activity in 50/60 neurons. This influence was expressed predominantly as a linear gain field, scaling task-related SC activity without changing the location of the response field (linear gain fields explained >/=20% of the variance in neural activity in approximately 50% of our sample). Smaller nonlinear modulations were also observed in roughly 30% of our sample. SC activity was equally likely to increase or decrease as the body was rotated to the side of neuronal recording and we found no systematic relationship between the directionality or magnitude of the linear gain field with recording location in the SC. We conclude that a signal conveying head-re-body position is present in the SC. Although the functional significance remains open, our findings are consistent with the SC contributing to a displacement-to-position transformation for oculomotor control.

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

“…This fraction was less than the fraction of neurons that show eye position gain modulation in all directions, 53% in SC (Van Opstal et al, 1995), 71% in posterior parietal cortex (Andersen et al, 1990), and 50% in the frontal eye fields (Cassanello and Ferrera, 2007), but comparable to the fraction (30%) of SC neurons that show collinear position gain-RF modulation (Van Opstal et al, 1995). This is consistent with the finding that the SC has an approximately equal probability of eye position gain modulation in different directions (Nagy and Corneil, 2010) and suggests that that eye position gain modulations extend to gaze in space (Brotchie et al, 1995). Our finding also supports neural network model predictions that SC neurons carry signals that could be used in a 3-D reference frame transformation (Salinas and Abbott, 2001; Smith and Crawford, 2005).…”

“…Our three-initial-target paradigm was designed to test whether the SC shows gaze position gain fields (Andersen and Mountcastle, 1983;Ben Hamed et al, 2002;Bremmer et al, 2002;Nagy and Corneil, 2010) orthogonal to the visuomotor tuning of its cells (Smith and Crawford, 2005). Since these target positions were set in a line in space (laboratory) frame (see Fig.…”

Recruitment of a contralateral head turning synergy by stimulation of monkey supplementary eye fields

“…Although the monosynaptic stretch reflex is much weaker than in limb muscles Rose 1988a, 1988b), there are numerous polysynaptic spinal and supraspinal routes (e.g., via the central cervical nucleus or vestibular nuclei) by which reafferent information from neck muscles can influence descending motor commands (see Richmond et al 2001a for review). Afferent neck muscle information also influences activity in numerous cortical and subcortical oculomotor targets (Fukushima et al 2010;Nagy and Corneil 2010;Snyder et al 1998). While the divergence of these ascending projections provides ample opportunity for interaction with descending motor commands, the nature of these interactions, and why they are influenced by head restraint, remains unclear.…”

“…Although SEF stimulation evoked neck muscle responses on almost all trials, such recruitment was not necessarily accompanied by overt head motion that exceeded our detection criteria. Given the head's substantial inertia, and reports describing subtle head motion far below traditional detection criteria (Chapman and Corneil 2011;Oommen and Stahl 2005), we conducted more precise analyses of head position and velocity on trials without overt head motion. These analyses directly compared head movement parameters during SEF stimulation with those during the same time interval on control trials without stimulation.…”

Motor output evoked by subsaccadic stimulation of primate frontal eye fields

“…Although the muscles that we recorded have a particularly dense complement of sensory receptors (17) that influences activity within oculomotor areas (18), it is difficult to conceive how sensations arising from evoked neck-muscle responses could produce the well-documented consequences of low-current FEF stimulation in extrastriate cortex. Such consequences are simply too rapid (5), widespread (19), and spatially restricted (4).…”