How do we distinguish motion in the world from similar retinal image displacements due to eye movements?
This problem has special importance in diseases such as vertigo and a variety of spatial orientation disorders,
where deficits in motion perception—including the suppression of self-motion—lead to devastating conse-
quences. Impaired balance and motion perception substantially impact people’s daily lives, hindering spatial
judgments and impeding performance during bodily motion tasks, such as ambulating or driving a vehicle. Until
we know how the brain differentiates self-motion from external motion, we will be unable to develop therapeutic
advances to address such disorders. Pioneering research in the 1960's - 90's—indeed the first published awake
non-human primate (NHP) vision study—asked whether early cortical neurons discerned ocular from external
motion, with the majority concluding that primary visual cortex (V1) neurons responded similarly to either type of
motion. These studies used different tasks for self-generated vs external motion conditions, however, meaning
that the respective neural responses evoked by either motion were not directly comparable. Thus, no research
to date has developed a model for how neurons in V1 respond to external vs. self-generated motion. Recent
work from the MPIs' labs, and others, has begun to use novel methods to directly compare self- vs real-motion
responses in V1. We propose a transformative study to leverage these new techniques to evaluate the responses
of V1 neurons to saccadic eye movements of all sizes under equivalent stimuli motions, with directly comparable
viewing tasks in all conditions, in all layers of V1 simultaneously, and to develop a model that links the specific
contributions of V1 circuits to perception. Our preliminary data suggests that V1 neurons can differentiate be-
tween self-generated and external motion, driving our hypotheses: 1) V1 neurons distinguish between self-
generated ocular motion vs. external retinal image motion, 2) an inhibitory feedback signal occurs during re-
sponses to self-generated motion to drive the discrimination process, and 3) V1 responses to eye movements
interact with responses driven by external motion in a nonlinear—though predictable—fashion, leading to both
physiological and perceptual effects on the detection of retinal motion. By comparing neurophysiological re-
sponses directly to perception in behaving NHPs, we will determine the contribution of V1 neurons to discerning
external vs self-generated motion, as well as the provenance of any feedback (and/or perhaps feedforward)
signals, using laminar analysis. These studies will establish the contributions of signals arriving to (or arising
within) different V1 layers, so as to dissociate external vs self- motion. We will create quantitative models (based
on our previously established models) using the new ground truth measurements from the proposed research,
to determine the precise neural and perceptual consequences of each V1 circuit involved. The studies will elu-
cidate loss of function in various oculomotor and neurological disorders and as such is directly relevant to the
research priorities of the Strabismus, Amblyopia, and Visual Processing program at the National Eye Institute.