Role of early visual cortex in trans-saccadic memory of object features

Abstract

Early visual cortex (EVC) participates in visual feature memory and the updating of remembered locations across saccades, but its role in the trans-saccadic integration of object features is unknown. We hypothesized that if EVC is involved in updating object features relative to gaze, feature memory should be disrupted when saccades remap an object representation into a simultaneously perturbed EVC site. To test this, we applied transcranial magnetic stimulation (TMS) over functional magnetic resonance imaging-localized EVC clusters corresponding to the bottom left/right visual quadrants (VQs). During experiments, these VQs were probed psychophysically by briefly presenting a central object (Gabor patch) while subjects fixated gaze to the right or left (and above). After a short memory interval, participants were required to detect the relative change in orientation of a re-presented test object at the same spatial location. Participants either sustained fixation during the memory interval (fixation task) or made a horizontal saccade that either maintained or reversed the VQ of the object (saccade task). Three TMS pulses (coinciding with the pre-, peri-, and postsaccade intervals) were applied to the left or right EVC. This had no effect when (a) fixation was maintained, (b) saccades kept the object in the same VQ, or (c) the EVC quadrant corresponding to the first object was stimulated. However, as predicted, TMS reduced performance when saccades (especially larger saccades) crossed the remembered object location and brought it into the VQ corresponding to the TMS site. This suppression effect was statistically significant for leftward saccades and followed a weaker trend for rightward saccades. These causal results are consistent with the idea that EVC is involved in the gaze-centered updating of object features for trans-saccadic memory and perception.

Visual working memory supports perceptual stability across saccadic eye movements.

“…In addition, Irwin and Robinson (2015) found that the detection of stimulus displacement across saccades was capacity-limited and largely (but not exclusively) focused on the saccade target. It has also been demonstrated that a saccade disrupts VWM task performance when transcranial magnetic stimulation (TMS) is applied to parietal or early visual cortex presumably because TMS prevents the neurons maintaining the visual representation of the memory from undergoing remapping, thereby disrupting memory for that object (Prime et al, 2008;Malik, Dessing, & Crawford, 2015).…”

Transsaccadic feature interactions in multiple reference frames: an fMRIa study

“…This ambiguity may therefore be a factor that led to modulation in both SMG and LOC. Dunkley et al (2016) accounted for the different responses in these regions (parietal RS vs. occipital RE) as the tendency of parietal cortex to respond better to Novel stimuli (Ardekani, Choi, Hossein-Zdeh, Porjesz, Tanabe, Lim et al, 2002; Linden, Prvulovic, Formisano, Voellinger, Zanella, Goebel, et al, 1999; Singh-Curry & Husain, 2009), versus occipital summation of pre- and post-saccadic feature information (Malik et al, 2015).…”

“…More specifically, the figure is summary of the cortical regions observed to be implicated within each spatial condition. Along with our results, we have also included areas that have been found to be involved in transsaccadic integration from previous studies (Prime et al, 2008; Prime et al, 2009; Tanaka et al, 2014; Malik et al, 2015). Lastly, we included links that represent possible underlying direct and indirect connections between the cortical regions we found here and the regions found in previous transsaccadic integration studies (Mishkin & Ungerleider, 1982; Sakata, Taira, Kusunoki, Murata & Tanaka, 1997; Culham & Kanwisher, 2001; James et al, 2002; Malach, Levy & Hasson, 2002; Grill-Spector et al, 2003; Goodale & Westwood, 2004).…”

“…Dorsolateral prefrontal cortex has been implicated in task switching between fixation and transsaccadic memory (Tanaka et al, 2014), so we speculate that it might play a similar role here, helping to select between these networks. Early visual cortex not only provides input to the visual system in general, it has been shown to be modulated by saccade signals (McFarland, Bondy, Saunders, Cumming & Butts, 2015; Sylvester, Haynes & Rees, 2005; Ross et al, 2001) and play a role in transsaccadic spatial updating of features (Malik et al, 2015). The parietal eye fields (located amongst our 3 networks) and frontal eye fields (modulated in our Spatially Incongruent task) may provide the saccade efference copy inputs for spatial updating, so again these signals might have been suppressed or gated differently in our non-Spatially Congruent tasks.…”

“…Little is known about the neural mechanisms subserving these different processes (Melcher & Colby, 2008; Cavanagh et al, 2010), but it has been shown that some aspects of transsaccadic integration can be disrupted by transcranial magnetic stimulation (TMS) over posterior parietal cortex (Prime et al, 2008), dorsolateral prefrontal cortex (Tanaka, Dessing, Malik, Prime & Crawford, 2014), and early visual cortex (Malik et al, 2015). Direct evidence for transsaccadic feature integration is scant, but monkey lateral intraparietal cortex (LIP) shows signs of modest spatial updating of rudimentary shape information (Subramanian & Colby, 2014).…”