Motion dependence of smooth pursuit eye movements in the marmoset

Abstract

Smooth pursuit eye movements stabilize slow-moving objects on the retina by matching eye velocity with target velocity. Two critical components are required to generate smooth pursuit: first, because it is a voluntary eye movement, the subject must select a target to pursue to engage the tracking system; and second, generating smooth pursuit requires a moving stimulus. We examined whether this behavior also exists in the common marmoset, a New World primate that is increasingly attracting attention as a genetic model for mental disease and systems neuroscience. We measured smooth pursuit in two marmosets, previously trained to perform fixation tasks, using the standard Rashbass step-ramp pursuit paradigm. We first measured the aspects of visual motion that drive pursuit eye movements. Smooth eye movements were in the same direction as target motion, indicating that pursuit was driven by target movement rather than by displacement. Both the open-loop acceleration and closed-loop eye velocity exhibited a linear relationship with target velocity for slow-moving targets, but this relationship declined for higher speeds. We next examined whether marmoset pursuit eye movements depend on an active engagement of the pursuit system by measuring smooth eye movements evoked by small perturbations of motion from fixation or during pursuit. Pursuit eye movements were much larger during pursuit than from fixation, indicating that pursuit is actively gated. Several practical advantages of the marmoset brain, including the accessibility of the middle temporal (MT) area and frontal eye fields at the cortical surface, merit its utilization for studying pursuit movements.

Methods for chair restraint and training of the common marmoset on oculomotor tasks

“…Saccades can be evoked by microstimulation within a subregion of frontal cortex in this species (Mott et al, 1910; Blum et al, 1982; Burish et al, 2008), further suggesting the existence of a FEF homologous to that of macaques (Bruce & Goldberg, 1985) and humans (Paus, 1996). Functionally, marmosets can be trained to make saccades (Mitchell et al, 2014; Nummela et al, 2016) and smooth pursuit eye movements (Mitchell et al, 2015) with metrics comparable to macaques and human participants, though they exhibit a decreased oculomotor range (Mitchell et al, 2014).…”

Why marmosets?

“…As discussed by Walker and colleagues in this issue, natural motor behaviors such as these make marmosets an exemplary model of voluntary motor control amongst primates (Walker et al, ). Likewise, marmoset visual behavior, while comparable to other primates in some dimensions, also exhibits distinct characteristics reflective of their unique evolutionary history (Mitchell et al, ; Mitchell and Leopold, ). Much of the value of marmosets as a neuroscientific model comes from leveraging these types of behavioral characteristics with a rapidly increasing set of techniques to examine the supporting neural processes.…”

The marmoset as a model system for studying voluntary motor control

“…In a study of the capacity for flexible control in a reinforcement learning‐based brain machine interface task, many of the analyses of experimental sessions were limited to 30 trials due to fidgeting marmosets (Pohlmeyer et al, ). In a couple of recent studies demonstrating the suitability of the common marmoset for studying the visual system, marmosets were found to perform 300–800 fixation trials but on average only 50 trials of a smooth pursuit paradigm (Mitchell et al, ). Studies reporting marmoset performance on different touch screen tasks varied from 60 to 150 trials in a session (Roberts et al, ; Clarke et al, ; Yamazaki et al, ).…”

“…The experimental challenges that marmosets present seem to compel refinement in techniques for using non‐human primates in behavioral and systems neuroscience research. As the marmoset becomes more established as a model species for the study of auditory processing, vocal production, active vision, and social behavior (Miller et al, , Mitchell et al, ), it seems like a good opportunity to design approaches utilizing newly available technology so that the precedents set for working with marmosets represent refinements on older standard operating procedures received from working with macaques.…”