The time course of the tonic oculomotor proprioceptive signal in area 3a of somatosensory cortex

Abstract

A proprioceptive representation of eye position exists in area 3a of primate somatosensory cortex (Wang X, Zhang M, Cohen IS, Goldberg ME. Nat Neurosci 10: 640-646, 2007). This eye position signal is consistent with a fusimotor response (Taylor A, Durbaba R, Ellaway PH, Rawlinson S. J Physiol 571: 711-723, 2006) and has two components during a visually guided saccade task: a short-latency phasic response followed by a tonic response. While the early phasic response can be excitatory or inhibitory, it does not accurately reflect the eye's orbital position. The late tonic response appears to carry the proprioceptive eye position signal, but it is not clear when this component emerges and whether the onset of this signal is reliable. To test the temporal dynamics of the tonic proprioceptive signal, we used an oculomotor smooth pursuit task in which saccadic eye movements and phasic proprioceptive responses are suppressed. Our results show that the tonic proprioceptive eye position signal consistently lags the actual eye position in the orbit by ~60 ms under a variety of eye movement conditions. To confirm the proprioceptive nature of this signal, we also studied the responses of neurons in a vestibuloocular reflex (VOR) task in which the direction of gaze was held constant; response profiles and delay times were similar in this task, suggesting that this signal does not represent angle of gaze and does not receive visual or vestibular inputs. The length of the delay suggests that the proprioceptive eye position signal is unlikely to be used for online visual processing for action, although it could be used to calibrate an efference copy signal.

Eye Position Encoding in Three-Dimensional Space: Integration of Version and Vergence Signals in the Medial Posterior Parietal Cortex

“…Several studies reported the presence of activations in the dorsalmost part of human POs for changes in the direction of gaze (Law et al, 1998;Williams and Smith, 2010), but to our knowledge only one reported activations in the dorsalmost POs for changes of eye vergence (Quinlan and Culham, 2007). All these findings well agree with present results (Xu et al, 2011). The horizontal dashed line indicates that ϳ80% of cells are already responding at that time.…”

“…Negative values represent responses starting before fixation onset, positive values responses starting after fixation start. As shown in Figure 8, ϳ80% of V6A cells discharged before the time the earliest proprioceptive signals arrive in somatosensory cortex (ϳ60 ms) (Xu et al, 2011). This suggests that, in most cases, in V6A the source of oculomotor signals is a corollary discharge.…”

“…The debate is still open on whether the eye position signal is derived from an efferent copy (corollary discharge) of a motor signal (Von Holst, 1954), or from a proprioceptive signal of eye muscles (Sherrington, 1918). In an elegant experiment, Goldberg (Wang et al, 2007) found a proprioceptive encoding of eye position in area 3a of the macaque somatosensory cortex, and recently the same group has showed that area 3a responses followed the eye position signal by ϳ60 ms (Xu et al, 2011). As the vast majority of fixation discharges in V6A started before this time point (Fig.…”

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

“…This raises the possibility that these data may have been contaminated by sensory and motor feedback signals during the gaze shift, and thus may not be "pure" SC signals. For example, eye and head position signals can alter visuomotor responses (Snyder et al, 1998;Xu et al, 2011) as fast as ϳ60 ms after an eye movement (Xu et al, 2011). To address this issue, we separated all of our data trials in all cells into a pre-saccade onset burst (Fig.…”

Eye Proprioception Used for Visual Localization Only If in Conflict with the Oculomotor Plan

“…Prompted by the recent discovery of an eye proprioceptive signal in area 3a in the monkey (Wang et al, 2007;Xu et al, 2011) and in the postcentral gyrus in humans (Balslev and Miall, 2008;Balslev et al, 2011) we have re-examined the question of whether eye proprioception contributes to locating stimuli in relation to the body in a patient (R.W.) with a focal lesion of the postcentral gyrus.…”