Beruflich Dokumente
Kultur Dokumente
Primates use two types of voluntary eye movements to track objects of interest: pursuit and saccades.
Traditionally, these two eye movements have been viewed as distinct systems that are driven automatical-
ly by low-level visual inputs. However, two sets of findings argue for a new perspective on the control of
voluntary eye movements. First, recent experiments have shown that pursuit and saccades are not con-
trolled by entirely different neural pathways but are controlled by similar networks of cortical and subcorti-
cal regions and, in some cases, by the same neurons. Second, pursuit and saccades are not automatic
responses to retinal inputs but are regulated by a process of target selection that involves a basic form of
decision making. The selection process itself is guided by a variety of complex processes, including atten-
tion, perception, memory, and expectation. Together, these findings indicate that pursuit and saccades
share a similar functional architecture. These points of similarity may hold the key for understanding how
neural circuits negotiate the links between the many higher order functions that can influence behavior and
the singular and coordinated motor actions that follow. NEUROSCIENTIST 11(2):124–137, 2005. DOI:
10.1177/1073858404271196
KEY WORDS Pursuit, Saccade, Eye movement, Attention, Perception
Primates make two kinds of voluntary eye movements to and cognitive processing capabilities of the primate cen-
place the retinal images of objects of interest onto the tral nervous system. The importance of these higher
fovea and to keep them there: saccades and pursuit. order processes, and the complexity of the underlying
Saccades are discrete ballistic movements that direct the mechanisms, pose both challenges and opportunities for
eyes quickly toward a visual target, thereby translating using voluntary eye movements as a model for under-
the image of the target from an eccentric retinal location standing the neural circuits involved in visuomotor con-
to the fovea within tens of milliseconds. Pursuit is a con- trol. This review highlights some recent findings that
tinuous movement that rotates the eyes smoothly and provide new perspectives on the functional organization
slowly to compensate for any motion of the visual target of these voluntary motor systems.
and thus minimizes the drift of the target’s image across
the retina that might otherwise blur the image and com- The Neural Pathways for
promise visual acuity. Pursuit and Saccades
Much of what we have learned about voluntary eye
movements over the past 40 years has involved treating Although the pursuit and saccadic systems have tradi-
these movements as visuomotor reflexes that act to min- tionally been viewed as anatomically distinct, more
imize visual “error” signals. Indeed, many species can recent evidence indicates that there is considerable over-
generate smooth optokinetic eye movements, which help lap in the neural pathways for pursuit and saccades. Both
stabilize the eyes during head and body movements by systems involve a similar set of areas in the cerebral cor-
minimizing the motion of the entire visual surround. tex (Fig. 1). For saccades, these cortical areas evaluate
However, when we move about in most natural environ- and update the locations of potential targets and provide
ments, it is impossible to eliminate the slip of images motor commands for saccades and include the lateral
across the retina. Instead, choices need to be made about intraparietal area (LIP), the frontal eye fields (FEFs),
which visual inputs have top priority. Primates appear to and the supplementary eye fields (SEFs). For pursuit,
be unmatched in their ability to identify individual cortical areas are involved in processing the visual
objects within a complex, dynamic visual scene and to motion and other control signals necessary for pursuit
track selected objects with their eyes. Voluntary eye and include the middle temporal (MT) and medial supe-
movements in primates are therefore not just a motor rior temporal (MST) areas and subregions of areas LIP,
phenomenon but depend on the sophisticated sensory FEF, and SEF. Thus, many of the same cortical areas are
involved in the control of both pursuit and saccades, but
each area contains separate subregions for the two types
Address correspondence to: Richard J. Krauzlis, Salk Institute for
Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA of movements, and the corresponding subregions are
92037 (e-mail: rich@salk.edu). interconnected to form a closely matched pair of cortical
Brain Stem
Fig. 1. Outline of the pathways for pursuit and saccadic eye
movements. Schematic diagram of the descending pathways It has been known for some decades that the motor com-
are depicted on a lateral view of the monkey brain. Shaded mands for saccades are constructed primarily by a circuit
regions indicate specific areas within the cerebral cortex, basal in the brain stem that generates the burst of neural activ-
ganglia, cerebellum, and brain stem, and arrows indicate the
anatomical connections between these areas. Regions demar- ity necessary to cause the rapid changes in muscle
cated with dashed lines indicate structures normally covered by force that propel saccades. The elements of this
the cerebral cortex. For clarity, not all relevant areas are depict- circuit are spread across several nuclei in the pons and
ed (e.g., ascending pathways are omitted), and arrows do not mesencephalon—the paramedian pontine reticular for-
always correspond to direct anatomical connections. CN = cau-
date nucleus (basal ganglia); FEF = frontal eye field; LIP = later-
mation (PPRF), the rostral interstitial nucleus of the
al intraparietal area; MT = middle temporal area; MST = medial medial longitudinal fasciculus (riMLF), and the nucleus
superior temporal area; PMN = brain stem premotor nuclei raphe interpositus (nRIP)—and contain several classes
(PPRF, riMLF, cMRF); PON = precerebellar pontine nuclei; SC = of saccade-related neurons (Luschei and Fuchs 1972;
superior colliculus (intermediate and deep layers); SEF = sup- Keller 1974; Sparks and Sides 1974; Henn and Cohen
plementary eye field; SNr = substantia nigra pars reticulate;
Verm = oculomotor vermis (cerebellum, lobules VI and VII); VN = 1976; Raybourn and Keller 1977; Van Gisbergen and
vestibular nuclei; VPF = ventral paraflocculus (cerebellum). others 1981; Henn and others 1984). Short-lead burst
neurons emit a burst of spikes whose precise timing
determines the amplitude of the saccade. Long-lead
burst neurons exhibit a prelude of activity before emit-
ting a saccade-related burst. Pause neurons in the nRIP
networks (Tian and Lynch 1996a, 1996b). Functional discharge steadily but stop firing during some or all sac-
imaging studies in humans also support the idea of par- cades (omnipause neurons [OPNs]). Several models
allel but distinct cortical pathways for pursuit and sac- (e.g., Scudder 1988) have suggested how these neurons
cades (Petit and Haxby 1999; Rosano and others 2002). might participate in saccade generation. A trigger signal,
These multiple cortical areas influence eye motor con- probably from the SC, causes OPNs to pause their firing
trol through several descending pathways. First, there are momentarily, which then disinhibits burst neurons. This
direct projections to eye-movement-related structures in disinhibition evokes a burst whose duration corresponds
the brain stem such as the superior colliculus (SC) and to the amplitude of the saccade; the burst duration is
premotor nuclei in the reticular formation (PMN). These controlled by a negative feedback circuit and is adap-
pathways, which have figured prominently in the control tively regulated in conjunction with the cerebellum.
of saccades, have been recently demonstrated to exist for New evidence indicates that parts of this brain stem
pursuit cortical areas as well (Yan and others 2001). circuit for saccades are also involved in the control of
There are also several less direct routes. One pathway pursuit. The primary brain stem nuclei for controlling
passes through the pontine nuclei to eye movement horizontal and vertical gaze (the PPRF, riMLF, and
regions of the cerebellum (oculomotor vermis, ventral cMRF) all receive direct inputs from the pursuit subre-
paraflocculus [VPF]), which access the output motor gion of the FEF as well as from the saccade-related sub-
nuclei for eye movements by projections to the vestibu- region (Yan and others 2001). Recent recording studies
lar nucleus and other brain stem motor nuclei (PMN). have shown that subsets of the neurons in these nuclei
For pursuit, this cortico-ponto-cerebellar route has been have pursuit-related as well as saccade-related activity.
traditionally considered the primary control pathway, For example, some burst neurons in the PPRF are active
whereas for saccades, it has been viewed primarily as a only during saccades, but a second category of burst
regulatory side loop. There are also descending path- neurons is active during both saccades and pursuit
ways involving nuclei of the basal ganglia, such as the (Missal and Keller 2001). Similarly, in the riMLF of the
caudate nucleus and the substantia nigra pars reticulata, cat, some burst neurons fire in relationship to eye veloc-
which exert their influence on eye movements through ity not only during saccades but also during pursuit
References
Albano JE, Mishkin M, Westbrook LE, Wurtz RH. 1982. Visuomotor
deficits following ablation of monkey superior colliculus. J
Neurophysiol 48:338–51.
Andersen RA, Snyder LH, Bradley DC, Xing J. 1997. Multimodal rep-
resentation of space in the posterior parietal cortex and its use in
planning movements. Annu Rev Neurosci 20:303–30.
Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P.
1999. Saccadic dysmetria and adaptation after lesions of the cere-
bellar cortex. J Neurosci 19:10931–9.
Basso MA, Krauzlis RJ, Wurtz RH. 2000. Activation and inactivation
Fig. 10. A hypothetical model of the functional organization of of rostral superior colliculus neurons during smooth-pursuit eye
voluntary eye movements. Rather than linking signals obtained movements in monkeys. J Neurophysiol 84:892–908.
from early visual processing steps directly to the motor outputs Basso M, Wurtz R. 1997. Modulation of neuronal activity by target
for pursuit and saccades (inset), the control of voluntary eye uncertainty. Nature 389:66–9.
movements involves a cascade of steps with several check- Basso MA, Wurtz RH. 1998. Modulation of neuronal activity in supe-
points that provide flexibility in how the movements are guided, rior colliculus by changes in target probability. J Neurosci
selected, and implemented. Evaluation of the sensory inputs 18:7519–34.
can be rapid but can also be influenced by higher order Bergeron A, Guitton D. 2002. In multiple-step gaze shifts: omnipause
processes such as perception, memory, and expected rewards (OPNs) and collicular fixation neurons encode gaze position error;
(sensory evaluation). The results from this evaluation proceed OPNs gate saccades. J Neurophysiol 88:1726–42.
along two tracks to influence the motor outputs. One track is Bergeron A, Matsuo S, Guitton D. 2003. Superior colliculus encodes
responsible for selecting the target and gating the motor distance to target, not saccade amplitude, in multi-step gaze shifts.
response (gating, target selection) and involves structures Nat Neurosci 6:404–13.
including the SC. The other track is responsible for providing Bisley JW, Goldberg ME. 2003. Neuronal activity in the lateral intra-
the drive signals that determine the metrics of the movements parietal area and spatial attention. Science 299:81–6.
(drive) and involves structures such as the cerebellum. In this Bogousslavsky J, Meienberg O. 1987. Eye-movement disorders in
model, the choice of whether to generate a pursuit movement brain-stem and cerebellar stroke. Arch Neurol 44:141–8.
or a saccade movement, or some combination of the two, is Bremmer F, Distler C, Hoffmann KP. 1997. Eye position effects in
not solely determined by the descending signals as in the tra- monkey cortex: II. Pursuit- and fixation- related activity in poste-
ditional view (inset) but instead depends on a comparison rior parietal areas LIP and 7A. J Neurophysiol 77:962–77.
between the descending signals and the current motor state Calton JL, Dickinson AR, Snyder LH. 2002. Non-spatial, motor-
(motor execution). specific activation in posterior parietal cortex. Nat Neurosci
5:580–8.
Cannon SC, Robinson DA. 1987. Loss of the neural integrator of the
oculomotor system from brain stem lesions in monkey. J
Neurophysiol 57:1383–409.
In contrast to earlier descriptions of the pursuit and Carello CD, Krauzlis RJ. 2004. Manipulating intent: evidence for a
saccade systems, the SC appears to be part of a shared causal role of the superior colliculus in target selection. Neuron
mechanism for selecting targets and perhaps triggering 43:575–83.
the two types of voluntary eye movements. It remains to Carpenter RH, Williams ML. 1995. Neural computation of log likeli-
hood in control of saccadic eye movements. Nature 377:59–62.
be clarified how this target-related activity is read out to Churchland MM, Lisberger SG. 2001. Shifts in the population
trigger the appropriate motor commands, especially response in the middle temporal visual area parallel perceptual and
because the SC does not mediate visual motion signals motor illusions produced by apparent motion. J Neurosci
for pursuit (Krauzlis 2004). It is also unclear whether the 21:9387–402.
SC simply applies a selection signal that is established Coe B, Tomihara K, Matsuzawa M, Hikosaka O. 2002. Visual and
anticipatory bias in three cortical eye fields of the monkey during
elsewhere—for example, the cerebral cortex—or an adaptive decision-making task. J Neurosci 22:5081–90.
whether it also plays a crucial role in the selection Cui DM, Yan YJ, Lynch JC. 2003. Pursuit subregion of the frontal eye
process itself, perhaps by regulating shifts of visual field projects to the caudate nucleus in monkeys. J Neurophysiol
attention. 89:2678–84.
Dias EC, Kiesau M, Segraves MA. 1995. Acute activation and inacti-
Many of the signals that guide pursuit and saccades vation of macaque frontal eye field with GABA-related drugs. J
come from a network of cortical areas and involve a vari- Neurophysiol 74:2744–8.
ety of processes important for the selectivity and guid- Dias EC, Segraves MA. 1999. Muscimol-induced inactivation of mon-
ance of voluntary eye movements: motor preparation, key frontal eye field: effects on visually and memory-guided sac-
attention, perception, and expected reward. Under most cades. J Neurophysiol 81:2191–214.