Neuronal Correlates of Multiple Top–Down Signals during Covert Tracking of Moving Objects in Macaque Prefrontal Cortex

Abstract

Abstract■ Resistance to distraction is a key component of executive functions and is strongly linked to the prefrontal cortex. Recent evidence suggests that neural mechanisms exist for selective suppression of task-irrelevant information. However, neuronal signals related to selective suppression have not yet been identified, whereas nonselective surround suppression, which results from attentional enhancement for relevant stimuli, has been well documented. This study examined single neuron activities in the lateral PFC when monkeys covertly tracked one of randomly moving objects. Although many neurons responded to the target, we also found a group of neurons that exhibited a selective response to the distractor that was visually identical to the target. Because most neurons were insensitive to an additional distractor that explicitly differed in color from the target, the brain seemed to monitor the distractor only when necessary to maintain internal object segregation. Our results suggest that the lateral PFC might provide at least two top-down signals during covert object tracking: one for enhancement of visual processing for the target and the other for selective suppression of visual processing for the distractor. These signals might work together to discriminate objects, thereby regulating both the sensitivity and specificity of target choice during covert object tracking. ■

Retrospective and prospective information coding by different neurons in the prefrontal cortex

“…The data from these neurons were presented in our previous paper (Figs. 5 and 8 of Matsushima and Tanaka, 2012). Among 85 neurons tested in the present study, 71 (84%) and 9 (11%) exhibited target-selective and distractor-selective responses, respectively.…”

“…We considered only neurons exhibiting a significant firing modulation depending on the stimulus location during the motion period in the covert tracking task, as in the previous study [20]. Briefly, the instantaneous firing rate was calculated for each stimulus location, which was filtered with a 2-D Gaussian kernel (σ = 2.5°, 20° square, 0.5° resolution) to obtain a response map.…”

“…All experimental protocols were approved in advance by the Animal Care and Use Committee of Hokkaido University. The procedures used for animal preparation are described elsewhere in detail [20,21]. Briefly, a pair of head holders was implanted on the skull using titanium screws and dental acrylic under general isoflurane anaesthesia.…”

“…1a). Animals were trained on the covert tracking, memory-guided saccade, and smooth pursuit tasks [20]. In the present study, we examined neuronal activity during the single target mode of the covert tracking task and during the memory-guided saccade trials.…”

Spatial and temporal adaptation of predictive saccades based on motion inference

“…Because the location of target reappearance relative to the fixation point varied from trial to trial (among seven possible locations), the alteration of predictive saccades in the present study likely reflected changes in sensory prediction based on motion inference rather than an adaptation of specific motor commands. Previous studies examined neuronal activity when animals kept track of an imaginary moving target 1,[10][11][12]59,60 or covertly moved attentional focus with visible objects 61,62 . In our predictive saccade paradigm, monkeys might also imagine a moving target behind the occluder and continuously update their attentional focus during target occlusion 63 .…”