Abstract
Searching for a visual object is known to be adaptable to context, and it is thought to result from the selection of neural representations distributed on a visual salience map, wherein stimulus-driven and goal-directed signals are combined. Here we investigated the neural basis of this adaptability by recording superior colliculus (SC) neurons while three female rhesus monkeys (Macaca mulatta) searched with saccadic eye movements for a target presented in an array of visual stimuli whose feature composition varied from trial to trial. We found that sensory-motor activity associated with distracters was enhanced or suppressed depending on the search array composition and that it corresponded to the monkey's search strategy, as assessed by the distribution of the occasional errant saccades. This feature-related modulation occurred independently from the saccade goal and facilitated the process of saccade target selection. We also observed feature-related enhancement in the activity associated with distracters that had been the search target during the previous session. Consistent with recurrent processing, both feature-related neuronal modulations occurred more than 60 ms after the onset of the visually evoked responses, and their near coincidence with the time of saccade target selection suggests that they are integral to this process. These results suggest that SC neuronal activity is shaped by the visual context as dictated by both stimulus-driven and goal-directed signals. Given the close proximity of the SC to the motor circuit, our findings suggest a direct link between perception and action and no need for distinct salience and motor maps.
Highlights
Our ability to select a visual object from amongst numerous alternatives is thought to be guided by a visual salience map (Cave and Wolfe, 1990; Findlay and Walker, 1999; Itti and Koch, 2000)
We recorded the activity of 42 sensory-motor neurons within the intermediate layers of superior colliculus (SC) while three rhesus monkeys reported with a saccadic eye movement which of the stimuli in a visual search display had a unique conjunction of features
To what extent can the feature sensitivity of sensory-motor neurons account for the observed biases in behavior? To answer this question and to determine the time course of this contextual modulation, we examined the relationship between the index of behavioral salience and the neuronal Modulation Index (MI) during three analysis epochs related to events within the discrimination process that were common across recording sessions despite the different response latencies: (1) when the neuron first responded to the visual stimulation, (2) when the neuron discriminated the target from any distracter, and (3) just prior to saccade initiation (Figure 6)
Summary
Our ability to select a visual object from amongst numerous alternatives is thought to be guided by a visual salience map (Cave and Wolfe, 1990; Findlay and Walker, 1999; Itti and Koch, 2000). The magnitude of each representation is related to the probability of selecting that object for further processing and, in the case of overt visual search, as a target for the saccadic eye movement. Stimulus discriminability is crucial to determining visual behavior when searching for a target stimulus amongst distracter stimuli (Treisman, 1988; Duncan and Humphreys, 1989; Wolfe et al, 1989): if discriminability is high, the representation of the search target on the visual salience map is significantly greater than those of distracter stimuli, resulting in a target that seems to “pop-out.”. Visual search studies have shown that both humans and monkeys are more likely to make saccades to stimuli that share features with the target of the current search session (Findlay, 1997; Motter and Belky, 1998) or of the previous one (Bichot and Schall, 1999b)
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