Two Types of Receptive Field Dynamics in Area V4 at the Time of Eye Movements?

Abstract

How we perceive the world as stable despite the frequent disruptions of the retinal image caused by eye movements is one of the fundamental questions in sensory neuroscience. Seemingly convergent evidence points towards a mechanism which dynamically updates representations of visual space in anticipation of a movement (Wurtz, 2008). In particular, receptive fields (RFs) of neurons, predominantly within oculomotor and attention related brain structures (Duhamel et al., 1992; Walker et al., 1995; Umeno and Goldberg, 1997), are thought to “remap” to their future, post-movement location prior to an impending eye movement. New studies (Neupane et al., 2016a,b) report observations on RF dynamics at the time of eye movements of neurons in area V4. These dynamics are interpreted as being largely dominated by a remapping of RFs. Critically, these observations appear at odds with a previous study reporting a different type of RF dynamics within the same brain structure (Tolias et al., 2001), consisting of a shrinkage and shift of RFs towards the movement target. Importantly, RFs have been measured with different techniques in those studies. Here, we measured V4 RFs comparable to Neupane et al. (2016a,b) and observe a shrinkage and shift of RFs towards the movement target when analyzing the immediate stimulus response (Zirnsak et al., 2014). When analyzing the late stimulus response (Neupane et al., 2016a,b), we observe RF shifts resembling remapping. We discuss possible causes for these shifts and point out important issues which future studies on RF dynamics need to address.

Pre-saccadic perception: Separate time courses for enhancement and spatial pooling at the saccade target

“…Our results are consistent with recent neurophysiological evidence [19], [20] that these two mechanisms have a different time course, with enhancement of the saccade target happening earlier (Experiment 1B) and maximum changes in spatial tuning (spatial compression) happening closer to saccade onset (Experiments 3B and 4). …”

Pre-saccadic remapping relies on dynamics of spatial attention

“…This indicates that forward remapping, like any other attentional process, requires some time. As we observed three separate focuses of attention (at the saccade target, cue and remapped location), we definitely ruled out the hypothesis that during saccade preparation attention spreads around the saccade target, as expected by the convergent remapping hypothesis 15,23,24 .…”

“…A more recent work indicated that the visual system may, in fact, implement both forward and convergent remapping of receptive fields in area V4 16,30 . As this combined approach has been criticized on technical grounds 23 , the neurophysiological results regarding the existence of forward remapping remain inconclusive.…”

“…Of note, the behavioral consequences of pre-saccadic changes in the spatial tuning of visual cells RF are unclear. Perhaps counterintuitively, recent computational neuroimaging modeling 34 has shown that increasing the neural spatial sampling at a particular position, similar as the over-sampling of the saccade target observed within convergent remapping studies 15,23,24 , results in a reduction of spatial uncertainty. Convergent remapping then does not necessarily yield a large spread of attention around the saccade goal 17 .…”

Spatial updating of attention across eye movements: A neuro-computational approach

“…Predictive remapping has been observed in many other areas: in extrastriate visual cortex (Nakamura & Colby, 2002), SC (Walker, Fitzgibbon, & Goldberg, 1995) and FEF (Umeno & Goldberg, 1997;Sommer & Wurtz, 2006). However, in these early studies predictive remapping was not clearly delineated from other receptive field shifts as discussed by Zirnsak, Lappe, and Hamker (2010) which triggered new experimental observations (Zirnsak, Steinmetz, Noudoost, Xu, & Moore, 2014;Neupane, Guitton, & Pack, 2016a, 2016bHartmann, Zirnsak, Marquis, Hamker, & Moore, 2017). This report focuses on modeling the neural substrates of the original predictive remapping phenomenon, as described by Duhamel et al (1992).…”