Macaque V1 Activity During Natural Vision: Effects of Natural Scenes and Saccades

Abstract

In the present study, we examined the way that scene complexity and saccades combine to sculpt the temporal response patterns of V1 neurons. To bridge the gap between conventional and free viewing experiments, we compared responses of neurons across four paradigms ranging from less to more natural. An optimal bar stimulus was either flashed into a receptive field (RF) or brought into it via saccade and was embedded in either a natural scene or a uniform gray background. Responses to a flashed bar tended to be higher with a uniform rather than natural background. The most novel result reported here is that responses evoked by stimuli brought into the RF via saccades were enhanced compared with the same stimuli flashed during steady fixation. No single factor appears to account entirely for this surprising effect, but there were small contributions from fixational saccades and residual activity carried over from the previous fixation. We also found a negative correlation with cells' response "history" in that a larger response on one fixation was associated with a lower response on the subsequent fixation. The effects of the natural background and saccades exhibited a significant nonlinear interaction with the suppressive effects of the natural background less for stimuli entering RFs with saccades. Together, these results suggest that even responses to standard optimal stimuli are difficult to predict under conditions similar to natural vision, and further demonstrate the importance of naturalistic experimental paradigms to the study of visual processing in V1.

Saccades during Object Viewing Modulate Oscillatory Phase in the Superior Temporal Sulcus

“…Sobotka et al (2002) reported a similar supra-additive interaction in IT and hippocampal evoked responses, when electrical microstimulation was delivered shortly following the end of a saccadic eye movement. These results are consistent with previous studies from early visual areas (Vinje and Gallant, 2000;Ibbotson et al, 2007Ibbotson et al, , 2008MacEvoy et al, 2008;Rajkai et al, 2008;Cloherty et al, 2010;Ito et al, 2011) and psychophysics (Burr et al, 1994;Diamond, 2002) that suggest visual processing is augmented following SEMs. To our knowledge, the present results are the first to show saccadic modulation in an object-selective region during viewing of faces and objects.…”

“…Although this is an attractive framework for interpreting the effect of SEMs on early visual areas (but see Gawne and Woods, 2003;MacEvoy et al, 2008), it is unlikely that object recognition operates on such context-free (or history-free) representations of retinal images. On the contrary, a hysteresis, or neural "memory" between fixations may be adaptive for transsaccadic integration (Melcher, 2005) and context-dependent processing (Buonomano and Maass, 2009).…”

“…The experimental convention of delaying stimulus onsets by hundreds of milliseconds relative to the end of SEMs may have led previous research to mischaracterize the functioning of the visual system during active vision, just as the experimental results presenting stimuli in isolation (i.e., stimulating only the classic receptive field) do not always generalize to stimuli embedded in contexts (Zipser et al, 1996;Gallant, 2000, 2002;Rolls et al, 2003;MacEvoy et al, 2008). Similarly, dissociating visual inputs from their natural temporal proximity to visual fixations is another experimental simplification that comes at the cost of external validity.…”

“…The neural basis of saccadic suppression has been explored in the LGN (Reppas et al, 2002) and motion-sensitive cortex (Thiele et al, 2002), and some of these studies also report that visual responses following saccades can be enhanced (Ibbotson et al, 2007(Ibbotson et al, , 2008Cloherty et al, 2010). For example, in primary visual cortex, fixation onset in darkness leads to a resetting of oscillations to a phase associated with high firing rates (Rajkai et al, 2008), and during visual stimulation, fixation onset leads to increased firing rates (Gallant et al, 1998;MacEvoy et al, 2008), spike synchronization (Maldonado et al, 2008;Ito et al, 2011), and sparseness (Vinje and Gallant, 2000). Whereas both saccadic suppression and enhancement following fixation are seen in many visual areas (for review, see Ibbotson and Krekelberg, 2011), they are poorly understood in object-selective visual areas.…”

Role of expected reward in frontal eye field during natural scene search

“…Our results also highlight the value of using natural scenes in vision experiments with nonhuman primates (Burman and Segraves 1994;Gallant et al 1998;MacEvoy et al 2008;Phillips and Segraves 2010;Rolls and Tovee 1995;Sheinberg and Logothetis 2001;Vinje and Gallant 2000). For instance, we were able to analyze saccades that landed near the target accidentally (without reward expectation), which would not occur in an experiment with simple stimuli.…”