Abstract
Sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies have demonstrated saccade-related activity in the dorsal pulvinar, and we have recently shown that many neurons exhibit postsaccadic spatial preference. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15°, 0°, 15°) in monkeys performing a visually cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed dependence on static gaze direction during initial and postsaccadic fixation, and might be signaling the position of the eyes in the orbit or coding foveal targets in a head/body/world-centered reference frame. The population-derived eye position signal lagged behind the saccade. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory, and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to postsaccadic fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in nonretinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually guided eye and limb movements.NEW & NOTEWORTHY Work on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. We show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.
Highlights
Information about eye position is ubiquitous in the primate brain and is critical for visually guided behavior
We demonstrate that about half of dorsal pulvinar cells are modulated by steady gaze position before visual cue onset and long after the saccade
A separate surgery was performed to implant a PEEK magnetic resonance imaging (MRI)-compatible chamber(s) allowing access to the pulvinar [monkey C, right hemisphere: center at 0.5A/14.5R mm, tilted Ϫ11P/ 27R degrees; monkey L, right hemisphere: center at Ϫ3.12P/20.2R mm, tilted Ϫ18P/37R degrees; monkey L, left hemisphere: center at Ϫ3P/20L, tilted Ϫ18P/-38L; the coordinates are relative to stereotaxic zero (A, anterior; P, posterior; L, left; R, right); the tilts are relative to the vertical axis normal to stereotaxic plane (P, posterior, top of the chamber tilted toward the back of the head; L/R, left/right, top of the chamber tilted toward the corresponding ear)]
Summary
Information about eye position is ubiquitous in the primate brain and is critical for visually guided behavior. Neurons modulated by the position of the eyes in the orbit have been reported in brain stem nuclei (Hernández et al 2019; Luschei and Fuchs 1972), superior colliculus (SC) (Campos et al 2006; Van Opstal et al 1995), inferior colliculus (Porter et al 2006), thalamus (Schlag-Rey and Schlag 1984; Tanaka 2007; Wyder et al 2003), cerebellum (Noda and Warabi 1982), and numerous cortical regions including visual and frontoparietal cortices (Andersen et al 1990; Bizzi 1968; Morris et al 2013; Squatrito and Maioli 1996; Trotter and Celebrini 1999; Wang et al 2007). The head is immobilized, and the position of eyes in the orbit is equivalent to gaze direction, or angle
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