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 micro-stimulation 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.

Significant advances in cognitive neuroscience can be achieved by combining techniques used to measure behavior and brain activity with neural modeling. Here we apply this approach to the initiation of rapid eye movements (saccades), which are used to redirect the visual axis to targets of interest. It is well known that the superior colliculus (SC) in the midbrain plays a major role in generating saccadic eye movements, and physiological studies have provided important knowledge of the activity pattern of neurons in this structure. Based on the observation that the SC receives localized sensory (exogenous) and voluntary (endogenous) inputs, our model assumes that this information is integrated by dynamic competition across local collicular interactions. The model accounts well for the effects upon saccadic reaction time (SRT) due to removal of fixation, the presence of distractors, execution of pro-versus antisaccades, and variation in target probability, and suggests a possible mechanism for the generation of express saccades. In each of these cases, the activity patterns of “neurons” within the model closely resemble actual cell behavior in the intermediate layer of the SC. The interaction structure we employ is instrumental for producing a physiologically faithful model and results in new insights and hypotheses regarding the neural mechanisms underlying saccade initiation.

Relative to when a fixated stimulus remains visible, saccadic latencies are facilitated when a fixated stimulus is extinguished simultaneously with or prior to the appearance of an eccentric auditory, visual, or combined visual-auditory target. In a study of nine human subjects, we determined whether such facilitation (the “gap effect”) occurs equivalently for the disappearance of fixated auditory stimuli and fixated visual stimuli. In the present study, a fixated auditory (noise) stimulus remained present (overlap) or else was extinguished simultaneously with (step) or 200 msec prior to (gap) the appearance of a visual, auditory (tone), or combined visual-auditory target 10° to the left or right of fixation. The results demonstrated equivalent facilitatory effects due to the disappearance of fixated auditory and visual stimuli and are consistent with the presumed role of the superior colliculus in the gap effect.

Two experiments examined saccadic reaction time (RT) in response to visual targets as a function of fixation offset condition (no offset; target simultaneous with offset and 200-msec offset-target SOA) in prosaccade and antisaccade tasks. The second experiment also included a condition in which saccades were made in response to verbal commands presented auditorally. To ensure that observers were equally prepared in each condition, auditory warning tones preceded target onset on every trial. The RT reduction associated with fixation offset (FOE, or gap effect) was identical with visual targets in the prosaccade task and in response to verbal signals, strongly implicating motor, rather than sensory, mechanisms in the FOE. The FOE in the antisaccade task was significant, but it was also significantly smaller than in the other tasks. We speculate that the reduced FOE in the antisaccade task may be due to the requirement to inhibit the superior colliculus when the target directed saccadic programs are, by instruction, erroneous.