A high-velocity eye movement or saccade is typically the first motor action we make to orient to an object of interest. While the neural mechanisms of saccade generation to stationary targets have been thoroughly investigated, very little is known about the neural control of interceptive saccades that acquire moving targets. Current dogma based on studies of saccades to stationary targets states that the visual and motor bursts in the superior colliculus (SC), a major hub in the oculomotor neuraxis, are represented as Gaussians; that the population activity is centered at the site encoding the target location and, equivalently, desired saccade vector; that its width remains invariant across different target locations and saccade vectors; and that these spatial features emerge from a balance of excitation and inhibition mediated through intrinsic, intra-laminar connectivity. Fundamentally non-overlapping mechanisms must be involved when the target is moving, because accurate interception can only occur if target velocity information is incorporated in the saccade command. We reason that as a moving target?s image streaks across the retina, activity sweeps across the SC too. We hypothesize that the population activity, which starts as a Gaussian to represent the initial visual response, becomes skewed as it sweeps across the SC; that the extent to which SC population activity is modified depends on the intra-laminar connectivity weights, the logarithmic map of visual space in SC, and target speed; that the altered spatial distribution persists during the peri-movement burst; and that an appropriate computational algorithm must be able to decode the saccade goal from the skewed population response. We propose to test these hypotheses using a combination of experimental and computational approaches.
Specific Aim 1 will employ an innovative method for simultaneously recording neural activity of many SC neurons within a functional layer in nonhuman primates performing oculomotor tasks and compare the spatiotemporal properties of population activity during saccades to stationary and moving targets (different speeds and directions).
Specific Aim 2 will construct a computational model that simulates population activity in SC and associated saccades to stationary and moving targets. We will employ a distributed architecture for the superficial and deeper layers of the SC and a lumped block-diagram circuit for the brainstem burst generator elements, like that done by Arai and colleagues (Neural Networks, 7:1115-1135, 1994). Collectively, these projects will provide an in-depth insight into the mechanisms for generation of interceptive saccades and enable a comparison with mechanisms of saccades to stationary targets.

Public Health Relevance

Oculomotor research has long been used to gain insights into ocular dysmotility including strabismus and neuropsychiatric disorders like schizophrenia and attention-deficit (hyperactive) disorder. It is also part of the standard battery of tests used to diagnose mild traumatic brain injury. Interceptive saccades can also be incorporated in these assessment criteria. In fact, considering the greater complexity of sensory to motor transformation required for intercepting a moving target, deficits may be detected more readily with this behavior. Also, a deeper insight into decoding algorithms used to convert population activity into a movement command has the potential to directly impact the development of biologically-inspired neural prostheses.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
2R01EY022854-05
Application #
9522756
Study Section
Mechanisms of Sensory, Perceptual, and Cognitive Processes Study Section (SPC)
Program Officer
Araj, Houmam H
Project Start
2013-05-01
Project End
2022-03-31
Budget Start
2018-04-01
Budget End
2019-03-31
Support Year
5
Fiscal Year
2018
Total Cost
Indirect Cost
Name
University of Pittsburgh
Department
Biomedical Engineering
Type
Biomed Engr/Col Engr/Engr Sta
DUNS #
004514360
City
Pittsburgh
State
PA
Country
United States
Zip Code
15213
Smalianchuk, Ivan; Jagadisan, Uday K; Gandhi, Neeraj J (2018) Instantaneous Midbrain Control of Saccade Velocity. J Neurosci 38:10156-10167
Goffart, Laurent; Cecala, Aaron L; Gandhi, Neeraj J (2017) The superior colliculus and the steering of saccades toward a moving visual target. J Neurophysiol 118:2890-2901
Jagadisan, Uday K; Gandhi, Neeraj J (2017) Removal of inhibition uncovers latent movement potential during preparation. Elife 6:
Jagadisan, Uday K; Gandhi, Neeraj J (2016) Disruption of Fixation Reveals Latent Sensorimotor Processes in the Superior Colliculus. J Neurosci 36:6129-40
Cecala, Aaron L; Smalianchuk, Ivan; Khanna, Sanjeev B et al. (2015) Context cue-dependent saccadic adaptation in rhesus macaques cannot be elicited using color. J Neurophysiol 114:570-84
Katnani, Husam A; Gandhi, Neeraj J (2013) Time course of motor preparation during visual search with flexible stimulus-response association. J Neurosci 33:10057-65