Elucidating the role of the oculomotor circuit in free viewing visual search

Project Summary
For almost 50 years, scientists have investigated the relationship between eye movement control and the activity
of neurons in the frontal eye field (FEF), superior colliculus (SC) and lateral intraparietal area (LIP). The general
findings of these studies have been that neurons in all three areas are important for eye movement behavior,
but they have identified very few differences between the areas, implying that they all do similar things. Recently,
a small number of labs have started using more naturalistic free-viewing behavioral tasks and have found a
number of substantive differences in neural responses across these areas, suggesting that they each play a
unique role. Based on these data, we formed a hypothesis about the roles of each area and how they may
function as a network to generate behavior. Briefly, we have proposed that LIP acts as simple priority map that
is constantly accessible, FEF activity controls the timing of saccades and SC activity represents the final decision
about where to look. In addition, a subset of neurons in FEF keeps track of where the animal has looked. Building
on this previous work, the current proposal has two main aims. The first is to fill in two gaps of our knowledge
that are essential in finalizing our hypothesis. As part of this aim, we propose to record from SC neurons in a
free viewing visual foraging task to confirm that SC activity is not affected by stimulus identity in ongoing search.
We also propose to record from FEF neurons in an even more natural version of our task to make sure that
suppression we have previously seen during maintained fixation is a mechanism for controlling the timing of eye
movements as opposed to a mechanism related to reward expectation. The results of these studies will refine
our hypothesis and set us up for the second main aim of the proposal, which is to test whether our hypothesized
roles are functionally valid. This second aim is broken into 3 components. In each, we will causally test aspects
of our hypothesis. In the first experiment, we will microstimulate LIP at different times to test whether the
suppression we have identified in FEF controls the flow of information from LIP to guide saccades. In the second
experiment, we will inactivate LIP while recording from FEF and SC. The results of this experiment will test the
hypothesis that LIP activity drives saccadic behavior via FEF and SC and, if it does not, these recordings should
identify which area does play a role in guiding behavior. In the third experiment, we will inactivate FEF while
recording from SC. This will allow us to test three additional aspects of our hypothesis: whether FEF activity
guides behavior and whether this is also represented in SCI; whether the tracking signal in FEF in functionally
relevant; and whether the activity in FEF is involved in controlling the temporal flow of saccades. These results
will solve a decades-long question of why we have multiple brain areas by providing a clear indication of what
the roles of LIP, FEF and SC are in everyday visual behavior. Given that patients across a broad spectrum of
neurological diseases have abnormal eye movement behavior, these results may aid in the development of
pharmacological or behavioral methods to combat these problems.

Grant Number: 5R01EY032863-04
NIH Institute/Center: NIH
Principal Investigator: James Bisley