Extraretinal Signals in MSTd Neurons Related to Volitional Smooth Pursuit

Abstract

. Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VORx1) and cancellation of the VOR (VORx0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity Յ 0.10 spike/s/°/s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SPrelated MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.

Different modulation of medial superior temporal activity across saccades: a functional magnetic resonance imaging study

“…This idea is derived from findings from earlier pursuit studies. During smooth pursuit, only MST receives extraretinal information [18], and MST can distinguish volitional from reflexive eye movements on the basis of this information [19]. Here, we used ES and visually guided saccades.…”

“…For example, one study reported that a patient with a parieto-occipital brain injury, including hMT + /V5, perceives the motion of a stationary world during pursuit [15]. Electrophysiological studies on monkeys showed that areas MT and MST can distinguish real object motion from retinal image motion [16,17], and activity of MST is modulated depending on volitionality [18,19]. The results of these studies and the possibility that pursuit and saccades share a neural substrate [20] allow us to hypothesize that the functional role of MST in visual motion processing during saccades differs from that of MT and that this difference is the cause of the discrepancy between the results of saccade studies.…”

Multimodal Coding of Three-Dimensional Rotation and Translation in Area MSTd: Comparison of Visual and Vestibular Selectivity

“…Shenoy et al (1999) reported that 20% of optic flow-sensitive MSTd neurons showed selectivity for yaw or pitch rotation while fixating a head-fixed target. However, Ono and Mustari (2006) reported no modulation of pursuit-sensitive MSTd neurons during yaw rotation in darkness. Previous studies of posterior parietal cortex had reported modulation during whole-body rotation in areas 7a/MST (Kawano et al, 1980(Kawano et al, , 1984Sakata et al, 1994) and in the lateral region of MST (Thier and Erickson, 1992a,b).…”

“…Furthermore, although MSTd responses to rotation in the absence of optic flow are often assumed to be vestibular in origin (but see, Ono and Mustari, 2006), this hypothesis has not been tested explicitly. Alternatively, tuning of MSTd neurons to inertial motion stimuli could arise, at least in part, from somatosensory signals.…”

Gaze-orientation during transient occlusion

“…The medial superior temporal (MST) area of the visual association cortex (V5a in humans), which processes velocity error signals when an object is visible, is known to receive extra-retinal inputs (Komatsu & Wurtz, 1989;Newsome, Wurtz, & Komatsu, 1988;Ono & Mustari, 2006). MST is implicated in the maintenance of smooth pursuit (Dürsteler & Wurtz, 1988) and a subset of neurons continues to be active when an object undergoes transient occlusion (Ilg & Their, 2003;Newsome et al, 1988).…”