Stephen Heinen

Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements

This report describes the behavior of neurons in the dorsomedial frontal cortex during smooth pursuit eye movements. Single neurons were recorded from monkeys while they tracked a small target that moved from the center of a screen outward. The firing rate of most cells was modulated during smooth pursuit eye movements, and often the activity peaked around pursuit initiation. Visual motion of the small target with the eyes fixed could activate pursuit neurons, but did not account for the total pursuit response. Neurons were also selective for the direction in which the animal was tracking, indicating that they were linked to the generation of the eye movements, and not to non-specific arousal effects. The results suggest that the dorsomedial frontal cortex participates in initiating smooth pursuit. It is proposed that the dorsomedial frontal cortex is part of a partial alternative path to the classic pursuit pathway that might be used to facilitate the initiation or control of eye movements beyond a simple reflexive response to retinal slip.

Human smooth pursuit direction discrimination.

The smooth pursuit system is usually studied using single moving objects as stimuli. However, the visual motion system can respond to stimuli that must be integrated spatially and temporally (Williams DG, Sekuler R. Vision Res 1984;24:55-62; Watamaniuk SNJ, Sekuler R, Williams DW. Vision Res 1989;29:47-59). For example, when each dot of a random-dot cinematogram (RDC) is assigned a new direction of motion each frame from a narrow distribution of directions, the whole field of dots appears to move in the average direction (Williams and Sekuler, 1984). We measured smooth pursuit eye movements generated in response to small (10 deg diameter) RDCs composed of 250 dynamic random dots. Smooth eye movements were assessed by analyzing only the first 130 ms of eye movements after pursuit initiation (open-loop period). Comparing smooth eye movements to RDCs and single spot targets, we find that both targets generate similar responses confirming that the signal supplied to the smooth pursuit system can result from a spatial integration of motion information. In addition, the change in directional precision of smooth eye movements to RDCs with different amounts of directional noise was similar to that found for psychophysical direction discrimination. These results imply that the motion processing system responsible for psychophysical performance may also provide input to the oculomotor system.

Spatial integration in human smooth pursuit

When viewing a moving object, details may appear blurred if the objects motion is not compensated for by the eyes. Smooth pursuit is a voluntary eye movement that is used to stabilize a moving object. Most studies of smooth pursuit have used small, foveal targets as stimuli (e.g. Lisberger SG and Westbrook LE. J Neurosci 1985;5:1662-1673.). However, in the laboratory, smooth pursuit is poorer when a small object is tracked across a background, presumably due to a conflict between the primitive optokinetic reflex and smooth pursuit. Functionally, this could occur if the motion signal arising from the target and its surroundings were averaged, resulting in a smaller net motion signal. We asked if the smooth pursuit system could spatially summate coherent motion, i.e. if its response would improve when motion in the peripheral retina was in the same direction as motion in the fovea. Observers tracked random-dot cinematograms (RDC) which were devoid of consistent position cues to isolate the motion response. Either the height or the density of the display was systematically varied. Eye speed at the end of the open-loop period was greater for cinematograms than for a single spot. In addition, eye acceleration increased and latency decreased as the size of the aperture increased. Changes in the density produced similar but smaller effects on both acceleration and latency. The improved pursuit for larger motion stimuli suggests that neuronal mechanisms subserving smooth pursuit spatially average motion information to obtain a stronger motion signal.

Perceptual and oculomotor evidence of limitations on processing accelerating motion

Psychophysical studies have demonstrated that humans are less sensitive to image acceleration than to image speed (e.g., Gottsdanker, 1956; Werkhoven, Snippe, & Toet, 1992). Because there is evidence that a common motion-processing stage subserves perception and pursuit (e.g., Watamaniuk & Heinen, 1999), either pursuit should be similarly impaired in discriminating acceleration or it must receive input from a system different from the one that processes visual motion for perception. We assessed the sensitivity of pursuit to acceleration or speed, and compared the results with those obtained in perceptual experiments done with similar stimuli and tasks. Specifically, observers pursued or made psychophysical judgments of targets that moved at randomly selected base speeds and subsequent accelerations. Oculomotor and psychophysical discrimination were compared by analyzing performance for the entire stimulus set sorted by either target acceleration or speed. Thresholds for pursuit and perception were higher for target acceleration than speed, further evidence that a common motion-processing stage limits the performance of both systems.

Timing and velocity randomization similarly affect anticipatory pursuit

Smooth pursuit eye movements are guided largely by retinal-image motion. To compensate for neural conduction delays, the brain employs a predictive mechanism to generate anticipatory pursuit that precedes target motion (E. Kowler, 1990). A critical question for interpreting neural signals recorded during pursuit concerns how this mechanism is interfaced with sensorimotor processing. It has been shown that the predictor is not simply turned-off during randomization because anticipatory eye velocity remains when target velocity is randomized (E. Kowler & S. McKee, 1987; G. W. Kao & M. J. Morrow, 1994). This study was completed to compare pursuit behavior during randomized motion-onset timing with that occurring during direction or speed randomization. We found that anticipatory eye velocity persisted despite motion-onset randomization, and that anticipation onset time was between that observed in the different constant-timing conditions. This centering strategy was similar to the bias of eye velocity magnitude away from extremes observed when direction or speed was randomized. Such a strategy is comparable to least-squares error minimization, and could be used to facilitate acquisition of a target when it begins to move. Centering was in some observers accounted for by a shift of eye velocity toward that generated in the preceding trial. The results make unlikely a model in which the predictor is disengaged by randomizing stimulus timing, and suggest that predictive signals always interact with those used in sensorimotor processing during smooth pursuit.

Anticipatory Movement Timing Using Prediction and External Cues

Animals often make anticipatory movements to compensate for slow reaction times. Anticipatory movements can be timed using external, sensory cues, or by an internal prediction of when an event will occur. However, it is unknown whether external or internal cues dominate the anticipatory response when both are present. Smooth pursuit eye movements are generated by a motor system heavily influenced by anticipation. We measured pursuit to determine how its timing was influenced when both a predictable event and a visual cue were present. Monkeys tracked a moving target that appeared at a constant time relative to the onset of a fixation point. At a randomized time before target onset, the fixation point disappeared, creating a temporal “gap” that cued impending target motion. We found that the gap onset cue and prediction of target onset together determined pursuit initiation time. We also investigated whether prediction could override the gap onset cue or vice versa by manipulating target onset and, hence, the duration of time that the animal had to estimate to predict it. When target motion began earlier, the pursuit system relied more on prediction to trigger a movement, whereas the cue was more often used when the target moved later. Pursuit latency in previous trials partially accounted for this behavior. The results suggest that neither internal nor external factors dominate to control the anticipatory response and that the relative contributions vary with stimulus conditions. A model in which neuronal anticipation and fixation signals interact can explain the results.

Neuroscience: rewiring the adult brain.

Arising from: S. M. Smirnakis et al. 435, 300–307 (2005); S. M. Smirnakis et al. replyAny analysis of plastic reorganization at a neuronal locus needs a veridical measure of changes in the functional output — that is, spiking responses of the neurons in question. In a study of the effect of retinal lesions on adult primary visual cortex (V1), Smirnakis et al. propose that there is no cortical reorganization. Their results are based, however, on BOLD (blood-oxygen-level-dependent) fMRI (functional magnetic resonance imaging), which provides an unreliable gauge of spiking activity. We therefore question their criterion for lack of plasticity, particularly in the light of the large body of earlier work that demonstrates cortical plasticity.

An Oculomotor Decision Process Revealed by Functional Magnetic Resonance Imaging

It is not known how the brain decides to act on moving objects. We demonstrated previously that neurons in the macaque supplementary eye field (SEF) reflect the rule of ocular baseball, a go/nogo task in which eye movements signal the rule-guided interpretation of the trajectory of a target. In ocular baseball, subjects must decide whether to pursue a moving spot target with an eye movement after discriminating whether the target will cross a distal, visible line segment. Here we identify cortical regions active during the ocular baseball task using event-related human functional magnetic resonance imaging (fMRI) and concurrent eye-movement monitoring. Task-related activity was observed in the SEF, the frontal eye field (FEF), the superior parietal lobule (SPL), and the right ventrolateral prefrontal cortex (VLPFC). The SPL and right VLPFC showed heightened activity only during ocular baseball, despite identical stimuli and oculomotor demands in the control task, implicating these areas in the decision process. Furthermore, the right VLPFC but not the SPL showed the greatest activation during the nogo decision trials. This suggests both a functional dissociation between these areas and a role for the right VLPFC in rule-guided inhibition of behavior. In the SEF and FEF, activity was similar for ocular baseball and a control eye-movement task. We propose that, although the SEF reflects the ocular baseball rule, both areas in humans are functionally closer to motor processing than the SPL and the right VLPFC. By recording population activity with fMRI during the ocular baseball task, we have revealed the cortical substrate of an oculomotor decision process.

The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects

The cerebellum is known to participate in visually guided eye movements. The cerebellar uvula receives projections from pontine nuclei that have been implicated in visual motion processing and the generation of smooth pursuit. Single-unit and lesion studies were conducted to determine how the uvula might further process these input signals. Purkinje cells and input fibers were recorded during a variety of visual and oculomotor paradigms. Most Purkinje cells were modulated in either an excitatory or inhibitory fashion by prolonged, horizontal optokinetic drum rotation. A small proportion of cells responded during smooth tracking of a small spot of light. As a paradox to the physiological data, lesions of the uvula produced a profound effect on smooth-pursuit eye movements. Initial eye velocity for pursuit in the direction contraversive to the lesion site was increased substantially following lesions in comparison with prelesion controls. The lesions also affected optokinetic nystagmus in the direction contraversive to the lesion, but not as drastically as they did pursuit. Overall the results suggest that the uvula is not in the neuronal pathway that directly controls pursuit, but instead serves to adjust the gain of this system as a result of abnormal periods of motion of the visual world.

The default allocation of attention is broadly ahead of smooth pursuit.

When moving through our environment, it is vital to preferentially process positions on our future path in order to react quickly to critical situations. During smooth pursuit, attention may be directed ahead with either a focused locus or a broad bias. We examined the 2D spatial extent of attention during a smooth pursuit task using both saccade (SRT) and manual (MRT) reaction times as measures of attentional allocation. Targets were flashed at various locations around current eye position while subjects pursued a moving target. Subjects made a saccade or pressed a button as soon as they perceived the target. Both SRTs and MRTs were shortest to targets flashed ahead of compared to behind the direction of pursuit across half of the visual field ahead of pursuit direction. Furthermore, we found an increase specific to SRTs at small target eccentricities directly ahead of pursuit, which may be related to an additional saccade trigger strategy; small saccades take longer to execute if smooth pursuit brings the eyes close to the target. In summary, both SRTs and MRTs revealed that attention is by default broadly allocated in the visual hemi-field ahead of the line of sight during smooth pursuit eye movements. This attentional bias may serve a predictive purpose for facilitating the processing of upcoming events.