Neural Circuitry of Smooth Pursuit

1. Tracking with Pursuit and Saccades

Smooth-pursuit eye movements support scrutiny of objects moving in space by matching eye velocity to target velocity in order to both reduce retinal blur of the moving object and facilitate its continued foveation. Smooth pursuit occurs when the FS selects a moving target or when a previously selected stationary target starts to move. However, target selection for pursuit also activates the saccadic system; hence, moving targets are usually tracked with a combination of smooth pursuit and saccades, with these two eye movement systems operating independently but sy-nergistically to track the same chosen target (Fig. 2). Their synergy reflects control by separate parameters of the target's trajectory. The principal impetus for smooth pursuit is target velocity (i.e., retinal slip), and the pursuit system continuously endeavors to eliminate retinal slip by matching eye velocity to target velocity. In contrast, the principal concern of the saccade system is target position (i.e., retinal error), and saccades are intermittently generated to eliminate retinal error by foveating the target.

However, this division of labor is not absolute. Smooth pursuit is modestly affected by positional errors: Ongoing pursuit accelerates in response to small retinal positional errors, and it is even possible to initiate smooth pursuit with an afterimage placed near the fovea (although eccentric afterimages are usually tracked with a succession of saccades). The pursuit system also responds to the rate of change in retinal slip

(i.e., acceleration). Thus, pursuit is a function of the zero-, first-, and second-order derivatives of the target's retinal image.

Conversely, the saccadic system attends to target velocity as well as location. Saccadic latency is shorter for targets moving centrifugally (away from the fixation point) and longer for targets moving centripe-tally. Moreover, saccades are usually directed to a predicted target location based on its position and velocity as acquired 100-200 msec before the saccadic movement starts.

Pursuit velocity ranges up to ~100°/sec; however, pursuit gain (defined, like VO and OK gain, as eye velocity/target velocity) is generally poor for target velocities above 25°/sec. When the pursuit gain is low, the eye will persistently fall behind the target and frequent, large ''catch-up'' saccades will be made; however, if gain is high ( b 1.0), then only a few, small saccades may be needed.

Interestingly, low smooth-pursuit gain is the principal symptom of the eye tracking dysfunction (ETD) of schizophrenia. Subsequent research has shown a cluster of oculomotor impairments that covary across the schizophrenic patient population and are often also present in first-degree relatives of schizophrenic patients. On the basis of the ETD and other cognitive aspects of schizophrenia, it has been hypothesized that schizophrenia reflects diminished frontal lobe function in general, and that the ETD specifically reflects impaired function in both the saccadic and the smooth-pursuit regions of the FEF.

2. Smooth Pursuit versus Optokinetic Following

Smooth pursuit can be confused with the OKR because both provide smooth, nonsaccadic ocular following in response to visual motion. However, the OKR is an automatic response to motion of large parts of the visual world (e.g., watching a train go by), whereas pursuit is the voluntary tracking of a discrete moving object (e.g., a bird flying across the sky).

In typical situations, smooth pursuit is in direct opposition to the OKR (and often to the VOR as well), and we choose to maintain foveation of the pursued target stimulus and reduce its retinal slip at the expense of increasing retinal blur of the rest of the visual field. For example, pursuit will need to override the OKR whenever tracking a target moving across a patterned background because as soon as pursuit starts the background necessarily becomes a stimulus for OKR in the opposite direction. Similarly, during combined head-eye tracking of a moving stimulus, the combined vestibulooptokinetic reflex must be overcome.

3. The Neural Pathway for Pursuit

The major pathways of the smooth-pursuit system are shown in Fig. 16. On the sensory and decision-making side, smooth pursuit is very much a neocortical behavior. It begins with the high-quality visual map in V1 that sends visual motion information into area V5 and other immediate extrastriate areas. Motion information is relayed to several other areas in the parietal and temporal lobe and to the smooth-pursuit zone of FEF. These cortical areas relay their visual motion signals and commands to oculomotor parts of the cerebellum, principally by way of their projections to the dorsolateral and medial pontine nuclei.

On the efferent side of the pursuit pathway, smooth movements are created by engaging the brain stem substrate for the slow-phase, compensatory part of VOR, much as visually guided saccades are made by engaging the mechanism that generates the quick phases of vestibuloocular nystagmus. Specifically, pursuit uses the VOR adaptation circuit that was shown in Fig. 8D. The key neurons are the Purkinje

Figure 16 Pathways for smooth-pursuit eye movements. The flow-chart shows that the smooth-pursuit part of the frontal eye field receives visual motion information from extrastriate motion areas, e.g., from the middle temporal area (MT, V5) and the medial superior temporal area (MST) and from parietal regions such as 7a and the ventral intraparietal area (VIP). INC, interstitial nucleus of Cajal; LGN, lateral geniculate nucleus; MVN, medial vestibular nucleus; NPH, nucleus prepositus hypoglossi; RTP, nucleus reticularis tegmenti pontis.

Figure 16 Pathways for smooth-pursuit eye movements. The flow-chart shows that the smooth-pursuit part of the frontal eye field receives visual motion information from extrastriate motion areas, e.g., from the middle temporal area (MT, V5) and the medial superior temporal area (MST) and from parietal regions such as 7a and the ventral intraparietal area (VIP). INC, interstitial nucleus of Cajal; LGN, lateral geniculate nucleus; MVN, medial vestibular nucleus; NPH, nucleus prepositus hypoglossi; RTP, nucleus reticularis tegmenti pontis.

cells in the floccular-nodular lobe and the parafloccu-lus regions of the cerebellar cortex. They carry a smooth-pursuit signal and effect pursuit by inhibiting vestibular nucleus neurons that in turn project to extraocular motoneurons. This pathway is both indirect, via the fastigial cerebellar deep nucleus, and direct from the Purkinje cells. In the context of the VOR, these projections from the cerebellum to the vestibular nuclei serve to adapt the VOR gain and offset. The smooth-pursuit system uses this pathway to temporarily create a vestibular imbalance in favor of desired pursuit direction, and thereby create a smooth eye movement. Cerebellar outputs may also aid pursuit by suppressing any opposing OKR evoked by the slip of the visual background once pursuit is underway as well as by suppressing any opposing VOR during combined head and eye pursuit.

4. Effects of Lesions in the Smooth-Pursuit Pathway

Neocortex is critical for smooth pursuit. Hemidecor-tication or large unilateral cortical lesions can cause a profound and permanent deficit of ipsilaterally directed pursuit in man and monkeys. Unilateral loss of V1 produces a permanent pandirectional loss of pursuit in response to motion in the contralateral hemifield. Discrete lesions in motion area V5 produce temporary pursuit deficits in restricted parts of the visual field (pursuit scotomas).

FEF lesions cause permanent ipsilateral pursuit deficits because each hemisphere's FEF is principally concerned with ipsilateral pursuit. Similar ipsiversive deficits, with profound reductions in both acceleration during pursuit initiation and steady-state pursuit velocity, follow lesions or temporary inactivation in the dorsolateral pontine nuclei. Finally, cerebellar lesions can cause severe and permanent pursuit deficits; in fact, smooth pursuit is the only eye movement type that is lost following cerebellectomy; other types of eye movements may be profoundly disturbed but are nevertheless still realized.

5. Sensory-to-Motor Transformation for Pursuit

Neurons throughout the pursuit pathway have been studied in the rhesus monkey. Similar to the saccadic system, neuronal activity in structures closer to the retina have obligatory responses to visual stimuli, but closer to the oculomotor nuclei the neural activity is more aligned to motor behavior. For example, neurons in V5 are highly selective for the direction of stimulus motion in their RFs. At the other end, the smooth eye velocity signal is elaborated in several pontocerebellar circuits, including the dorsolateral and the medial pontine nucleus and the nucleus reticularis tegmenti pontis, together with cerebellar pursuit areas (the flocculus, paraflocculus, and dorsal vermis). Many neurons in these structures respond as a function of pursuit velocity.

The critical step in this sensorimotor transformation underlying pursuit is provided by the neurons that respond to target motion, but only if it is selected for foveation/pursuit. The smooth-pursuit zone of FEF (Fig. 14) is a candidate site. It lies downstream from V5 and other areas that provide most of the visual motion information for smooth pursuit, but upstream from pontocerebellar and brain stem circuits that effect pursuit movements. Microstimulation in the pursuit FEF elicits smooth eye movements (usually ipsiver-sive), and many FEF pursuit cells discharge to the motion of a pursuit target over most of the visual field but discharge little to moving targets that are not pursued. An FEF pursuit cell is shown in Fig. 17; notice that it also discharged during predictive pursuit at the end of sinusoidal tracking and that reversible inactivation at this FEF site caused a immediate deficit in ipsilateral smooth pursuit.

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