Contribution of the Primate Superior Colliculus to Inhibition of Return

Abstract

Abstract& The phenomenon of inhibition of return (IOR) has generated considerable interest in cognitive neuroscience because of its putative functional role in visual search, that of placing inhibitory tags on objects that have been recently inspected so as to direct further search to novel items. Many behavioral parameters of this phenomenon have been clearly delineated, and based on indirect but converging evidence, the widely held consensus is that the midbrain superior colliculus (SC) is involved in the generation of IOR. We had previously trained monkeys on a saccadic IOR task and showed that they displayed IOR in a manner similar to that observed in humans. Here we recorded the activity of single neurons in the superficial and intermediate layers of the SC while the monkeys performed this IOR task. We found that when the target was presented at a previously cued location, the stimulus-related response was attenuated and the magnitude of this response was correlated with subsequent saccadic reaction times. Surprisingly, this observed attenuation of activity during IOR was not caused by active inhibition of these neurons because (a) they were, in fact, more active following the presentation of the cue in their response field, and (b) when we repeated the same experiment while using the saccadic response time induced by electrical microstimulation of the SC to judge the level of excitability of the SC circuitry during the IOR task, we found faster saccades were elicited from the cued location. Our findings demonstrate that the primate SC participates in the expression of IOR; however, the SC is not the site of the inhibition. Instead, the reduced activity in the SC reflects a signal reduction that has taken place upstream. &

Dorsal and Ventral Parietal Contributions to Spatial Orienting in the Human Brain

“…A more plausible explanation thus could be that IPS stimulation might have acted by extending the duration of endogenous early facilitatory effects, masking or even interrupting IOR, which ac- cording to event-related recordings operates in the system, even if masked in behavioral measures (Wascher and Tipper, 2004;Chica and Lupiáñez, 2009). The interference of IPS stimulation on the exogenous task found in our study fits well with the hypothesized role of the posterior parietal cortex, in concert with the superior colliculus (SC) (Dorris et al, 2002), as part of the circuitry underlying IOR. The SC is a brainstem structure receiving retinal input, implicated in saccade execution and heavily connected to the FEF (Wurtz and Albano, 1980) and the posterior parietal cortex (Clower et al, 2001).…”

Inhibition of return, gap effect and saccadic reaction time to a visual target

“…However, a recent electrophysiological study (19) has shown that the primate SC participates in the expression of IOR, but is not the site of inhibition. Instead, the reduced response of collicular neurons reflects a signal reduction elicited by the cue that has occurred upstream, probably in the posterior parietal cortex (19). The possible participation of cortical structures in IOR may explain the similarities between the ocular and manual expression of IOR.…”

“…This is an unexpected result because the rostral colliculus is involved in ocular fixation (20). However, a recent electrophysiological study (19) has shown that the primate SC participates in the expression of IOR, but is not the site of inhibition. Instead, the reduced response of collicular neurons reflects a signal reduction elicited by the cue that has occurred upstream, probably in the posterior parietal cortex (19).…”

“…However, the SC is not the site of inhibition. Instead, the reduced response of collicular neurons reflects a signal reduction elicited by the cue that has occurred upstream, probably in the posterior parietal cortex (19).…”

“…18 and 19). However, the SC might not be sufficient IOR, gap effect and saccadic reaction time for IOR to be observed (19). Single-unit recording has shown that when the target was presented at a previously cued location the response of collicular neurons was attenuated and the magnitude of this response was correlated with subsequent SRT.…”