Saccade Target Selection in the Superior Colliculus During a Visual Search Task

Abstract

Because real-world scenes typically contain many different potential objects of interest, selecting one goal from many is clearly a fundamental problem faced by the saccadic system. We recorded from visual, movement, and visuo-movement (VM) neurons in the superior colliculus (SC) of monkeys performing a reaction-time visual-search task requiring them to make saccades to an odd-colored target presented with distractors. First, we compared the responses of SC neurons in search with their responses when a single target was presented without distractors (single-stimulus task). Consistent with earlier reports, initial visual activity was smaller in search than in the single-stimulus task, while movement-related activity in the two tasks was comparable. Further experiments showed that much of the reduction in the initial visual response during search was due to lateral inhibition, although a top-down task-related component was also evident. Although the initial visual activity did not discriminate the target from the distractors, some neurons showed a biphasic pattern of visual activity. In VM burst neurons, the second phase of this activity was significantly larger when the target, rather than a distractor, was in the response field. We traced the time course of target/distractor discrimination using receiver operating characteristic (ROC) analysis and found that VM burst neurons, VM prelude neurons, and pure movement neurons discriminated the target from distractors before saccade onset but that phasic and tonic pure visual neurons did not. We also examined the relationship between target/distractor discrimination time and saccade latency. Discrimination in VM burst neurons having a biphasic pattern of visual activity and in many VM prelude neurons occurred after a consistent delay that did not depend on saccade latency, suggesting that these neurons are involved in target selection as well as movement initiation. In contrast, VM burst neurons lacking a biphasic pattern of visual activity, pure movement neurons, and a subset of VM prelude neurons discriminated the target at a time that was well correlated with saccade latency, suggesting that this latter group of neurons is involved in triggering movement execution but not in target selection. Thus a mix of signals likely related to target selection and movement initiation co-exists in different groups of SC neurons. This suggests that certain types of SC neurons participate in the target selection process and that the SC as a whole represents a gateway for target selection signals to be converted into a saccadic command.

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

“…Indeed, this is exactly what we found in our intermediate reference frame analysis: a distribution of coding schemes centered around Te. This agrees with the view that the final visuomotor reference frame transformation is performed at a lower premotor level (Klier et al, 2001), leaving a role for the SC in higher-level spatial functions such as target selection (Basso and Wurtz, 1998;McPeek and Keller, 2002;Müller et al, 2005;Shen and Paré, 2007) and attentional allocation (Carello and Krauzlis, 2004;Lovejoy and Krauzlis, 2010).…”

“…Nevertheless, the current study also suggests that the saccade-related burst in SC activity primarily encodes visual target direction during head-unrestrained gaze shifts, despite considerable variations in eye/head kinematics. This is consistent with a role for the SC in higher-level functions such as target selection (Basso and Wurtz, 1998;McPeek and Keller, 2002;Müller et al, 2005;Shen and Paré, 2007) and attentional allocation (Kustov and Robinson, 1996;Carello and Krauzlis, 2004;Lovejoy and Krauzlis, 2010). However, since some of our neurons preferred G over T, our data do not exclude the possibility that the SC is partially involved in the early computations for gaze kinematics (and see the next section on Gain modulation).…”

Dynamic integration of information about salience and value for saccadic eye movements

“…The representation of a salience map has been associated with different brain areas; among them are areas in the early visual cortex V1 and V4 and oculomotor-related areas, such as the LIP area, the frontal eye fields (FEF), and the superior colliculi (SC) (23)(24)(25)(26)(27). The LIP area, FEF, and SC are of functional importance for eye movement planning and execution, as demonstrated by microstimulation in these areas (28)(29)(30).…”

Prefrontal Cortex Deactivation in Macaques Alters Activity in the Superior Colliculus and Impairs Voluntary Control of Saccades

“…1996; Ignashchenkova et al, 2004), target selection (Horwitz and Newsome, 2001;McPeek and Keller, 2002), and choice (Thevarajah et al, 2009).…”