Active exploration (Active Sensing) in the visual domain uses two different processes: overt exploration that occurs about 3-5 times per second via moving the eyes, and covert search utilizing a `spotlight' that continuously scans the visual scene by moving to new locations at a rate of up to 20 times per second. While overt exploration is considered a rhythmic behavior, the spotlight of attention utilized during covert search has traditionally been characterized as a single sustained spatial mechanism. Recent behavioral evidence has called this concept into question.!First, the attentional spotlight, rather than being sustained, flashes rhythmically, sampling the visual environment at frequencies in the theta band (4-8Hz), with alternating temporal windows of relatively enhanced and diminished processing. Second, our recent behavioral work supports the existence of two spatial mechanisms, concurrently sampling the visual scene: (i) a fixed spotlight that rhythmically samples the most relevant location, and (ii) a moving spotlight that rhythmically monitors less relevant locations. Thus, covert attention used during Active Sensing may fall into the class of rhythmic behaviors just like its overt counterpart. In this project, we will investigate the neural basis of rhythmic covert attention and relate it to neuronal oscillatory rhythms underlying overt search by recording simultaneously from multiple nodes of the network utilized during visual exploration in monkeys trained in both covert and overt attention tasks. In Experiment 1, we will use laminar multielectrodes to simultaneously record laminar profiles from area V4 and FEF and from their interconnected zone in the pulvinar nucleus of the thalamus. Monkeys will be trained on a visual threshold detection task that parametrically examines rhythmic sampling from a location at which attention is sustained as well as rhythmic monitoring of one or two locations outside the focus of attention. We will specifically emphasize rhythmic cortico-cortical intra-areal interactions and the influence of the pulvinar in mediating communication between cortical areas. In Experiment 2, we will record from these areas while monkeys are engaged in an overt search task to detect visual objects; this task will be combined with the visual detection task that induces rhythmic sampling at an attended location used in Experiment 1 to directly compare mechanisms utilized during overt and covert search. We will also obtain ECoG signals from low impedance electrodes placed over the two cortical areas to relate these signals to the laminar profile acquired simultaneously. Such comparison will be beneficial for interpreting results from Project 1 that proposes to use similar tasks in human ECoG studies. Our findings, and those of Project 4, which uses similar tasks and recording methods to study auditory Active Sensing, will feed data to biophysical cellular- circuit modeling in Project 5. Across the Center, our studies will aim at establishing a neural basis for rhythmic overt and covert explorative behavior in the visual and auditory domains, and at constructing robust models that represent Active Sensing' s neuronal substrates at local circuit and brain network scales.
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