Neuronal Control of Eye Movements - part 5 docx

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Prof. Dr. P. Thier
Department of Cognitive Neurology, Hertie Institute for Clinical Brain Research
Hoppe-Seyler Strasse 3
DE–72076 Tübingen (Germany)
Tel. ϩ49 7071 2983057, Fax ϩ49 7071 295326, E-Mail
Straube A, Büttner U (eds): Neuro-Ophthalmology.
Dev Ophthalmol. Basel, Karger, 2007, vol 40, pp 76–89
Smooth Pursuit Eye Movements and
Optokinetic Nystagmus
Ulrich Büttner, Olympia Kremmyda
Department of Neurology, Ludwig-Maximilians University, Munich, Germany
Abstract
Smooth pursuit eye movements are used to track small moving visual objects and
depend on an intact fovea. Optokinetic nystagmus is the oculomotor response to large mov-
ing visual fields. In addition, the ocular following response is considered, which reflects
short latency, involuntary eye movements to large moving visual fields. This chapter will
consider the general characteristics and the anatomical and physiological basis of these eye
movements. It will conclude with disorders, particularly those seen in clinical investigations.
Copyright © 2007 S. Karger AG, Basel
General Characteristics
Smooth Pursuit Eye Movements
The performance of smooth pursuit eye movements (SPEM) is a voluntary
task and depends on motivation and attention. SPEM are only found in species
with a fovea and are used to maintain a clear image of small moving visual
objects on the retina. The latency for the initiation of SPEM is 100–150 ms [1],
which is generally shorter than for a saccade. During initiation (eye accelera-
tion) SPEM depend mainly on visual signals, and during maintained pursuit on
a ‘velocity memory’ signal [2].
In contrast to saccades, SPEM are usually considered as ‘slow’ eye move-

ments, although velocities above 100Њ/s can be reached [man: 3; monkey: 4].
Cats, with a coarse area centralis can track larger stimuli only up to 20Њ/s [5]. In
man, there is a clear age dependence of SPEM [6]. They are already present in
4-week-old infants and reach a gain close to 1 at 3 months [7]. As a rule, maxi-
mal velocity decreases every year by 1Њ/s starting at the age of 20 [3]. There
seems to be no further decline above the age of 75 [8].
Smooth Pursuit and Optokinetic Nystagmus 77
Under normal circumstances, tracking of small moving visual objects is
done by eye and head movements. Head movements induce the vestibulo-ocular
reflex (VOR), which drives the eyes in the direction opposite to the eye move-
ments. During visual tracking the VOR has to be suppressed, and it is assumed
that the central nervous system actually generates a smooth pursuit signal to
cancel the VOR [9]. Thus, a SPEM deficit is generally accompanied by
impaired VOR suppression.
Usually SPEM are tested with sinusoidal stimuli which only refer to steady
state conditions. They are different from the initial 20–40 ms, when SPEM are
independent from stimulus parameters. To account for the different motor pro-
grams on a neuronal level for SPEM generation, often the step-ramp (Rashbass)
paradigm is used. So far, only few clinical studies addressed the question of
partial dysfunction in SPEM generation [10].
Both SPEM and saccades are voluntary eye movements. Traditionally they
have been considered as two distinct systems. However, it is becoming increas-
ingly evident that both types of eye movements share similar anatomical networks
at the cortical and subcortical level. These networks are presumably used for
selection processes involving attention, perception, memory and expectation [11].
Optokinetic Response
Large moving visual fields (with the head stationary) lead to slow com-
pensatory eye movements. These eye movements are driven by the optokinetic
system. During continuous motion of the visual surround, fast resetting eye
movements occur, which are basically saccades. The combination of slow com-

pensatory and fast resetting eye movements is called optokinetic nystagmus
(OKN), the direction being labeled after the fast phase.
Two components can be distinguished in the generation of the slow com-
pensatory phase [12]. One is called the ‘direct’ component, because it occurs
directly after the onset of the optokinetic stimulus and is considered to reflect
the ocular following response (OFR) [13]. It can best be demonstrated by the
rapid increase in slow-phase eye velocity after the sudden presentation of a
constant optokinetic stimulus. In contrast, the second component is called the
‘indirect’ component, because it leads to a more gradual increase in slow-phase
eye velocity during continuous stimulation. The best demonstration of the ‘indi-
rect’ component alone is optokinetic after-nystagmus (OKAN) – the nystagmus
that continues in the dark after the light has been turned off [12]. The ‘indirect’
or ‘velocity storage’ component can be related to concomitant activity changes
in the vestibular nuclei [14–16].
There is also some evidence that the ‘direct’ component is more involved
in translational optical flow in contrast to rotational optical flow for the ‘indi-
rect’ component [17].
Büttner/Kremmyda 78
In birds and lateral-eyed animals (rat, rabbit) the optokinetic response
consists almost entirely of the ‘indirect’ component. In the monkey, both
components are well developed, and maximal OKN velocities can reach more
than 180Њ/s [12, 18]. In contrast, in humans the ‘indirect’ component is
often weak (as indicated by OKAN), variable, and sometimes virtually miss-
ing [3, 19].
Maximal OKN velocities in the horizontal plane seldom exceed 120Њ/s in
humans and can be mainly related to the ‘direct’ component. Clinically, values
above 60Њ/s are considered normal [3]. There seems to be some age-related
decline in OKN responses for subjects aged Ͼ75 years [8]. At constant stimulus
velocities below 60Њ/s, the gain (eye/stimulus velocity) is about 0.8 [20].
Responses can still be obtained at sinusoidal stimulation above 1 Hz [21]. OKN

is also used to determine residual visual capacities in patients with severe motor
and intellectual disabilities [22].
Vertical OKN has been less intensively investigated. In general, vertical
OKN is slower than horizontal OKN and upward stimulation is more effective
than downward stimulation [23]. At the bedside, normal function can be
assumed as long as up and down OKN can be elicited. In the upright body posi-
tion, vertical OKAN is often missing or only present after upward optokinetic
stimulation [23]. With a rotating visual field, also torsional OKN with a low
gain (Ͻ0.2) can be elicited [24, 25].
Ocular Following Response
The immediate involuntary response to a large moving visual field is
called OFR. OFR in humans can have latencies as short as 60–70 ms, which are
shorter than those for SPEM. The size of the visual stimulus and the involuntary
character are further features to distinguish these eye movements. The OFR is
functionally linked to the translational VOR in contrast to OKN being related to
the rotational VOR [26]. Experiments in humans with moving square waves and
stimuli, in which the fundamental frequency of the square wave pattern was
removed, revealed that the eyes always move in the direction of the strongest
Fourier component, which is in the latter case the third harmonic. Under these
conditions the eyes can move in the opposite direction (due to the third har-
monic) of the movement of the general stimulus pattern [27]. Longer interstim-
ulus intervals can reverse the direction of the OFR [27]. These findings support
the hypothesis that visual motion detection for OFR is sensed by low-level
(energy-based) rather than feature-based (high-level) mechanisms [28]. The
middle temporal visual area (MT) and medial superior temporal visual area
(MST) appear to be early cortical stages involved in motion responses [29] and
in the initiation of OFR [30].
Smooth Pursuit and Optokinetic Nystagmus 79
Anatomy and Physiology
Smooth Pursuit Eye Movements

SPEM are the result of a complex visuo-oculomotor transformation
process, which involves many structures at the cortical as well as the cerebellar
and brainstem level [31, 32] (fig. 1). Frontal as well parietotemporal areas are
involved in smooth pursuit generation. The main areas posterior to the central
sulcus are the occipital cortex, the MT, the MST and the parietal cortex. With
lesions in the occipital cortex SPEM are abolished in the contralateral hemi-
field, when step-ramp stimuli are used [33]. However, with sinusoidal stimuli
SPEM remain intact due to the use of predictive SPEM properties and the spar-
ing of the macular projection.
Area 17 (occipital cortex) projects ipsilaterally to the MT (also called V5).
Neurons here have large receptive fields and encode the speed and the direction
of moving visual stimuli [34]. In the monkey, small lesions in the extrafoveal
part of the MT cause a deficit in SPEM initiation [35]. Based on functional
MRI, the MT in humans is located posterior to the superior temporal sulcus at
the parieto-temporo-occipital junction (Brodmann areas 19, 37 and 39) [36].
Frontal cortex
FEF, SEF
NRTP
Cerebellum
Vermis
FOR
Posterior cortex
MT, MST
PN
MVN, Y group
Floccular region
VPFL (FL)
Motoneurons
Fig. 1. Major SPEM-related structures and their connections. The cortical structures
(FEF, SEF, MT, MST) project via pontine structures (NRTP, PN) to the cerebellum [vermis,

VPFL (FL)]. From here, activity travels via deep cerebellar nuclei (FOR) and the vestibular
nuclei (MVN, Y group) to the oculomotor neurons in the brainstem. The anatomical pathway
from the FOR to the motoneurons is not well established (dashed line). There is some evidence
that the frontal cortex projects mainly via NRTP to the vermis and the posterior cortex mainly
via PN to the FL
Büttner/Kremmyda 80
The MST is adjacent to the MT, from where it receives an input. Also neurons
in the MST have large receptive fields and are well suited for the analysis of
optic flow [37]. In contrast to the MT, MST neurons can still be active without
retinal motion being present [38]. Experimental lesions of the MST produce a
SPEM deficit to the ipsilateral side in both visual hemifields [39]. The MST
appears to be largely involved in SPEM maintenance, whereas the MT is more
involved in SPEM initiation [32]. In man, the homologues of the MT and MST
are also adjacent to each other at the occipitotemporoparietal junction.
Over the last years, it became increasingly clear that also the frontal eye
fields (FEFs) and the supplementary eye field (SEF) in the frontal cortex are
involved in SPEM generation. Both structures, FEF and SEF, have been known
for their involvement in saccade generation. The SPEM-area of the FEF is
anatomically distinct of the saccade area [40]. Lesions in monkeys [41] and
humans [42] cause a severe ipsidirectional deficit particularly in predictive
aspects of SPEM. Interestingly, optokinetic responses can be preserved [43].
Also the SEF appears to be involved in predictive aspects of SPEM [44]. It has
been suggested that SEF is particularly involved in the planning of SPEM [32].
Evidence starts to emerge that also the basal ganglia [45] and the thalamus
are involved in SPEM control. Anatomically, it has been shown that both the
saccade and the SPEM-related division of the FEF project to separate areas in
the caudate nucleus [46]. Also, the saccade and the SPEM-related division of
FEF receive different thalamic inputs [47]. Recent single unit studies indicate
that the thalamus regulates and monitors SPEM by providing a corollary dis-
charge to the cortex [48].

There is some evidence that FEF projects mainly to the nucleus reticularis
tegmenti pontis (NRTP) [49] and MT/MST more strongly to the dorsolateral
pontine nuclei (DLPN) [50] (fig. 1). The DLPN projects only to the cerebellum.
Here afferents terminate in lobulus VI and VII of the vermis (oculomotor ver-
mis; OV) [51] and the paraflocculus [49]. Neuronal activity in DLPN would
preferentially allow a role in maintaining steady-state SPEM [49]. Discrete
chemical lesions in DLPN in monkeys produce mainly an ipsilateral SPEM
deficit [52]. NRTP projects to the OV [51] and to a lesser degree to the
paraflocculus [53]. Neurons here encode primarily eye acceleration, which
would indicate a larger role of NRTP in smooth pursuit initiation [49].
In the cerebellar cortex, the floccular region (FL) and OV are most inten-
sively investigated in relation to SPEM. In monkeys, lesions in both the FL [54]
and OV [55] lead to SPEM deficits. OV lesions in monkeys lead to a smooth
pursuit gain reduction particularly during the first 100 ms (in the open-loop
period). Deficits are also seen in humans after OV lesions [56]. The OV projects
to the caudal part of the fastigial nucleus (fastigial oculomotor region; FOR)
(fig. 1), where lesions also cause a SPEM deficit (to the contralateral side) [57].
Smooth Pursuit and Optokinetic Nystagmus 81
The FL projects directly to the vestibular nuclei, from where SPEM signals
can reach the oculomotor nuclei. It is not quite clear yet, how the SPEM signals
from FOR reach the oculomotor nuclei.
There is some evidence for two parallel pathways from the cortex for
SPEM. The parietotemporal structures (MT, MST) project preferentially to the
pontine nuclei, which in turn send afferents to the FL. In contrast, the FEF
mainly sends signals via NRTP to the OV and FOR (fig. 1). The functional dif-
ferences for these two routes at all levels still have to be determined.
Optokinetic Nystagmus
As outlined above, here only the ‘indirect’ or ‘velocity storage’ component
of OKN will be considered. Although the ‘velocity storage’ component can be
transmitted solely via brainstem pathways, it is important to remember, that

these pathways are under cortical control. Bilateral occipital lesions lead to a
loss of optokinetic responses in both humans [58] and monkeys [59].
Fibers from the retina terminate in the brainstem in the nuclei of the acces-
sory optic tract (AOT) and the nucleus of the optic tract (NOT), only the latter
being part of the pretectal nuclear complex [60]. Both AOT [61] and NOT [50]
receive cortical inputs. Being located in the mesencephalon, they project to
more caudal brainstem areas like the pontine nuclei, NRTP, the inferior olive,
nucleus prepositus hypoglossi and the vestibular nuclei. Neurons in AOT and
NOT have large receptive fields and respond best to large textured stimuli mov-
ing in specific directions [62].
It is well known that vestibular nuclei neurons not only respond to vestibu-
lar stimulation in the dark but also to large moving visual stimuli that cause
OKN [15, 14]. During OKAN, vestibular nuclei activity and slow-phase eye
velocity change in parallel.
The cerebellum does not appear to play a major role in mediating the
‘indirect’ component of OKN [63]. Cerebellectomy in cat does not greatly
affect optokinetic responses. The nodulus and uvula appear to have an
inhibitory effect. In the monkey, ablation maximizes the ‘indirect’ component
[64]. This lack of inhibition is considered as the cause for periodic alternating
nystagmus.
Ocular Following Response
Single unit recordings and chemical lesion studies indicate that the OFR is
mediated by a pathway including the MST, DLPN and the ventral paraflocculus
(VPFL), i.e. pathways involved in SPEM. Detailed analysis of the neural activity
suggests that the MST locally encodes the dynamic properties of the visual
stimulus, whereas the VPFL provides the motor command for OFR [65].
Büttner/Kremmyda 82
Disorders
Smooth Pursuit Eye Movements
Cortex

Both frontal and parietal lesions in patients lead to SPEM deficits [66].
Lesions of the MT region cause a deficit [67] similar to that seen in monkeys
[68]. Moving stimuli within the contralateral visual field defect cannot be ade-
quately tracked independent of the movement direction, whereas saccades to
the defective area remain intact. In contrast, lesions of the neighboring MST
lead to a directional (ipsiversive) deficit independent of the retinal location.
Also lesions of the FEF lead to an ipsiversive SPEM deficit [69]. The MT, MST,
FEF and SEF project via the internal capsula to the pons. Accordingly, an
ipsiversive deficit is also seen after lesions in the internal capsula [70].
Pontine Structures
Lesions of the pontine nuclei lead to a predominantly ipsiversive SPEM
deficit [71, 72]. However, even bilateral lesions of the pontine nuclei do not
abolish SPEM. This might reflect that also the NRTP is involved in SPEM gen-
eration. Smooth pursuit deficits in ‘progressive supranuclear palsy’ [73] and
spinocerebellar ataxia types 1, 2 and 3 [74] have also been related to lesions of
the pontine structures.
Cerebellum
In the cerebellar cortex, lesions of the OV and the FL lead to SPEM
deficits. Patients with cerebellar ataxia and bilateral vestibulopathy show a
reduced SPEM gain [75]. A total loss of SPEM is only seen when both struc-
tures are lesioned (total cerebellectomy, monkey). In the OV, SPEM- as well as
saccade-related neurons are found. Lesions always lead to related deficits [76]
(table 1). A bilateral lesion of the OV leads to hypometric saccades and SPEM
with a reduced gain. This is also seen in patients [77, 78]. Effects of unilateral
lesions have not yet been described in patients.
The Purkinje cells of the OV project to the FOR and have an inhibitory
effect. Consequently, a bilateral lesion of the FOR leads to hypermetric saccades.
This should be combined with an increased SPEM gain (gain Ͼ1). In this case,
back up instead of catch up saccades should occur during SPEM. However, this
pattern is only rarely seen [79] (fig. 2). Still, a patient with a severe hypermetria

due to a bilateral FOR lesion showed highly normal values with a SPEM gain
close to 1 [80]. Experimental (monkey) unilateral lesions lead to a SPEM gain
reduction and hypometric saccades to the contralateral side and normal SPEM
and hypermetric saccades to the ipsilateral side [57] (table 1).
Smooth Pursuit and Optokinetic Nystagmus 83
Table 1. The effect of cerebellar midline lesions and lateral medullary infarction on
SPEM and saccades
Smooth pursuit Saccades
unilateral bilateral unilateral bilateral
ipsi- contra- ipsi- contra-
OV ⇓ hypo- hyper- hypo-
(lobulus VI, VII)
FOR normal ⇓ normal hyper- hypo- hyper-
Rostral cerebellum ⇓⇓ hypo- hyper-
(cereb. outflow)
Lateral medulla normal ⇓ hyper- hypo-
(Wallenberg)
In general, a reduced SPEM gain is combined with hypometric saccades. This is not the
case for lesions in the rostral cerebellum since not only FOR efferents but also pathways to
and from the FL are affected.
H (NORM)
T
RT
LT
10º
H (MUSC)
*
*
*
*

*
Fig. 2. Effect of transient inactivation by local muscimol injection in the right FOR on
SPEM. T ϭ Target position; H (NORM) ϭ horizontal eye position before muscimol injec-
tion; H (MUSC) ϭ horizontal eye position after muscimol injection; RT ϭ right; LT ϭ left.
During rightward movements, the SPEM gain is Ͼ1 and back-up saccades (marked by aster-
isks) occur. During leftward movements, the smaller gain is corrected by catch-up saccades;
from Fuchs et al. [79].
Büttner/Kremmyda 84
Efferent pathways from the FOR cross immediately to the other side before
they enter the brainstem. Accordingly, patients with a lesion to the rostral cere-
bellum show saccadic contrapulsion [81], i.e. the reverse pattern of a unilateral
FOR lesion. It is usually found with lesions in the territory of the superior cere-
bellar artery. In this case, saccades to the contralateral side are hypermetric and
hypometric to the ipsilateral side. However, SPEM show a low gain in both
directions [82] occasionally more pronounced to the ipsilateral side [83]. The
reason probably is that lesions of the rostral cerebellum do not only affect the
FOR pathways but also the pathways to and from the FL.
Lesions of the FL lead to a partial SPEM deficit, more pronounced to the
ipsilateral side. In contrast to OV and FOR lesions, the SPEM deficit is usually
combined with gaze-evoked nystagmus due to a gaze holding deficit [84].
Medulla
The most common ischemic lesion of the brainstem is the lateral medulla
infarction (Wallenberg’s syndrome); in patients, it always (100%) leads to ocu-
lomotor deficits [85]. This includes a SPEM deficit to the contralateral side
[86]. As pointed out above for OV and FOR lesions, also this deficit corre-
sponds with hypometric saccades to the contralateral side (table 1). It is postu-
lated that this deficit is caused by interruption of olivocerebellar pathways after
their crossing in the medulla [87, 88] (fig. 3).
Optokinetic Nystagmus
For patients, there are no good methods available to test the ‘indirect’ com-

ponent of OKN in isolation. One possible method would be to test their OKAN.
However, even in normals OKAN can be missing [19]. On the bedside, usually
a handheld optokinetic cylinder is rotated for several seconds in one direction.
This however only activates the ‘direct’ (smooth pursuit-related) component,
since the time is not sufficient to provide a substantial contribution of the ‘indi-
rect’ component [16]. When optokinetic stimuli are used, a side difference of up
to 20Њ/s for the maximal velocity is still considered normal [89]. Pathological
side differences are more obvious with the use of smaller stimuli [90]. For the
monkey, it could be shown that mesencephalic lesions in the pretectum lead to
a reduction in the ‘indirect’ component to the ipsilateral side. Also the OKAN
in this direction is missing or reduced [91]. There is also some evidence that in
addition pretectal lesions can affect the ‘direct’ component [92]. Clinical
reports on this topic are still missing.
Smooth Pursuit and Optokinetic Nystagmus 85
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?
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Prof. Dr. U. Büttner
Department of Neurology
Klinikum Grosshadern, Marchioninistrasse 15
DE–81377 Munich (Germany)
Tel. ϩ49 89 7095 2560, Fax ϩ49 89 7095 5561, E-Mail

Straube A, Büttner U (eds): Neuro-Ophthalmology.
Dev Ophthalmol. Basel, Karger, 2007, vol 40, pp 90–109
Disconjugate Eye Movements
Dominik Straumann
Neurology Department, Zurich University Hospital, Zurich, Switzerland
Abstract
To foveate targets in different depths, the movements of the two eyes must be disconju-
gate. Fine measurements of eye rotations about the three principal axes have demonstrated
that disconjugate eye movements may appear not only in the horizontal, but also in the verti-
cal and torsional directions. In the presence of visual targets, disconjugate eye movements
are driven by the vergence system, but they may also appear during vestibular stimulation.
Disconjugate eye movements are highly adaptable by visual disparities, but under normal
condition the effects of adaptation only persist when one eye is covered. Finally, disorders of
the brainstem and cerebellum may lead to abnormal disconjugate eye movements that are
often specific for the topography of the lesion. This chapter reviews the literature on the
phenomenology of disconjugate eye movements over the last 15 years.
Copyright © 2007 S. Karger AG, Basel
The goal of normal disconjugate eye movements is to direct the corre-
sponding retinal points of the two eyes to a visual object that is nearer or farther
than the previous object. Such vergence movements can also be smooth when
the object of interest moves slowly in depth. Both disparity and accommoda-
tion-vergence synkinesis can drive vergence movements. Recently, it has also
been shown that perceived depth alone elicits vergence eye movements [1].
Geometrically, binocular movements are disconjugate, if amplitude and/or
direction are unequal for both eyes. Considering the full kinematics of eye rota-
tions, the term ‘direction’ includes ocular rotation about the line of sight, which
is an important degree of freedom to ensure extrafoveal retinal correspondence.
If one takes into account the rigid geometric specifications for 3-D – i.e. hori-
zontal, vertical, and torsional – binocular rotations, it is not surprising that nor-
mal eye movements are generally disconjugate when subjects view near targets.

As we shall see, even eye movements for foveation of targets at infinity exhibit
some disconjugacy due to neural and mechanical factors.
Disconjugate Eye Movements 91
This paper reviews the literature on the phenomenology, including
pathophenomenology, of disconjugate eye movements over the last 15 years.
Horizontal Vergence Movements
Under natural viewing conditions, horizontal vergence movements are
usually dysmetric, i.e. moving gaze from a near to a far target leads to exces-
sive convergence, and moving gaze from a far to a near target to insufficient
convergence [2]. The degree of this physiological vergence weakness can
be reduced by increased attention [3] and instruction [4], but vergence is
always less precise than version [5]. In subjects with strong monocular pre-
ference, vergence movements are typically associated with small horizontal
saccades [6].
Upon symmetric step stimulation with horizontal disparity, convergence is
usually faster than divergence [7]. While the dynamics of convergence move-
ments is independent of target location, divergence movements become faster
the closer the initial target is to the eyes [8]. When visual feedback is eliminated
during vergence, the position trajectories are step-like, not smooth. This open-
loop response consists of a pulse-like or transient component and a step-like or
sustained component [9, 10]. While both components are adaptable, only the
pulse-like component influences the dynamics of the adapted vergence
response [11]. Experiments eliciting vergence movements by velocity steps of
horizontal disparities suggest that the vergence open-loop response may origi-
nate from monocular visual pathways [12].
Disparity-driven convergence eye movements frequently show large asym-
metries, which vary from trial to trial and are usually compensated in the later
phase of the convergence movement [13]. While this later phase probably uses
visual feedback, the initial phase seems to be preprogrammed [14]. The occa-
sional appearance of two closely spaced high-velocity vergence movements in

response to disparity supports the notion that the initial vergence component is
evoked by an internal, not visual, feedback mechanism that is switched on and
off, analogous to the saccadic system [15, 16].
Small or large dichoptic displays that are counterphasically oscillated in
the horizontal direction elicit dynamic convergence/divergence [17]. Brief hor-
izontal (or vertical) disparity steps of 2Њ or less evoke short-latency vergence
movements, which are enhanced when the stimulus is presented shortly after a
saccade [18–20]. Similar vergence movements with short latencies are also
driven by radial flow [21]. When vergence movements with or without accom-
panying saccades are elicited with a gap period before target onset, vergence
latency decreases significantly [22].
Straumann 92
Vertical Vergence Movements
A vertical prism placed in front of one eye induces divergent eye move-
ments in the vertical direction. Training with vertical prisms can increase the
vertical fusional amplitude, predominantly by enhancing the motor, not the sen-
sory component [23]. The motor capability to fuse vertical disparities increases
with convergence. This increase is due to the motor component, while the sen-
sory component for far and near viewing is practically the same [24]. Similarly,
skew deviation associated with static counterroll (intorting eye hypertropic)
increases with convergence [25].
Vertical fusion is accompanied by conjugate torsion toward the higher eye
[26], a pattern that qualitatively resembles the one seen in patients with dissoci-
ated vertical deviation [27]. Whether the binocular torsion associated with
vertical fusion is mediated by the superior oblique muscles (SO) [26] or is of
central origin [28] remains to be answered. 3-D eye movement trajectories
during vertical fusion suggest that patients with congenital trochlear nerve
palsy use predominantly the vertical recti, while patients with acquired
trochlear nerve palsy show various patterns of vertical and oblique eye muscle
activations [29].

Dichoptic counterphasic oscillation of displays in the vertical direction
elicits vertical vergence [30]. These movements show increased gain and
reduced phase lag with larger stimulus diameter, which contrasts horizo-
ntal dichoptic display oscillation, in which display diameter is less important
[31].
Cyclovergence
Spontaneous fluctuation of torsional eye position is generally conjugate,
i.e. cyclovergence is considerably more stable than cycloversion [32]. Opposite
cyclorotation of the images presented to the two eyes evokes static cyclover-
gence, which adds to the eye position-dependent cyclovergence [33]. The latter
results from the outward rotations of Listing’s planes during convergence (see
below).
Dynamic cyclovergence can be elicited by fusible visual patterns projected
to each eye separately and oscillated out of phase in the frontal plane [34, 35].
The gain of dynamic cyclovergence is highest for low frequencies and low
amplitudes and therefore is appropriate to correct for drifts in binocular stereo-
scopic alignment, which are both slow and small [35]. Occlusion of the central
area does not influence the gain of cyclovergence, although the gain of
cycloversion decreases [36].
Disconjugate Eye Movements 93
Listing’s Law during Convergence
For the following considerations, eye positions need to be described three-
dimensionally with a horizontal, vertical, and torsional component. Since rota-
tions are noncommutative, the most convenient conventions, such as rotation
vectors or quaternion vectors, express every eye position as a single axis rota-
tion from a reference position. Accordingly, vergence is then defined as the
rotation that transforms the left eye position into the right eye position [37].
Rotation or quaternion vectors hold a specific 3-D orientation in the head.
Listing’s law states that, in the absence of dynamic vestibular stimulation, these
3-D vectors all lie in one plane, so-called Listing’s plane. In the absence of con-

vergence, the Listing’s planes of the two eyes are relatively parallel and oriented
approximately frontal. With convergence the planes rotate outward [38–41], i.e.
they ‘swing out like saloon doors’ [42]. In other words, the primary positions of
the two eyes diverge during convergence [43]. Among the cited studies, the angle
of the outward rotation of the Listing’s planes varies considerably and amounts
roughly to about 1/4 (range: 0.16–0.43) of the convergence angle (fig. 1).
An explanation of why the Listing’s planes rotate outward during conver-
gence has to consider both visual and motor variables [44]. Tweed [45] pro-
posed a most compelling hypothesis that is based on an optimal compromise
between visual and motor variables: The visual variable is the maximal align-
ment of images in the visual plane on the two retinas irrespective of gaze direc-
tion; the motor variable is to keep rotation about the line of sight as close as
possible to the zero vergence primary position. Since the amount of cyclovergence
varies with gaze elevation when the Listing’s planes are rotated outward, stere-
ograms that critically depend on the relative torsional orientation of the two
retinas are only visible at a specific gaze elevation [46]. Hence, ocular motor
control plays an important role in depth vision.
␣
␣/4 ␣/4
Fig. 1. Top view of binocular Listing’s planes during far (left) and near (right) viewing.
Each Listing’s plane rotates temporally by a quarter of the vergence angle (␣).
Straumann 94
MR images demonstrate that rectus pulleys in converging eyes are slightly
extorted [47]. The outward rotation of Listing’s plane, however, cannot be
explained by this change of the rectus pulleys and therefore must be due to vari-
ations of oblique muscle innervations. The convergence-induced outward rota-
tion of Listing’s planes does not depend on whether convergence is induced by
a stereogram, a horizontal prism, or an accommodative stimulus [48–50]. The
orientation of Listing’s planes can, however, be modified by phoria adaptation
(see below).

Vergence movements with the eyes at various elevations lead to different
torsional components that can be explained by the vergence-modulated orienta-
tion of Listing’s plane [41]. Accordingly, during pure vergence movements with
gaze elevated or depressed, the eyes rotate about an axis which is orthogonal to
the gaze direction [51]. This is different from the orientation of rotation axes
during saccades, which tilt in the direction of gaze by only half the gaze angle
[52]. During asymmetric vergence movements, e.g. when foveating a target
moving along the line of sight of one eye, monocular torsion is less stable than
cyclovergence and varies between convergence and divergence [53, 54]. Pitch
head impulses while the eyes are converging on a near target in front of one eye
lead to torsional movement components in both the adducting and the straight
ahead viewing eye [55]. This effect corresponds to a modification of ocular
rotation axes due to the convergence-induced outward rotation of Listing’s
planes.
The Listing’s planes in patients with acquired trochlear nerve palsy are not
symmetric; the plane of the affected eye is rotated outward, as if this eye were
converging [56]. In congenital trochlear nerve palsy, the orientation of Listing’s
plane of the affected eye is normal; thus, congenital trochlear nerve palsy is not
due to changed function of a single extraocular eye muscle [56]. In patients
with acquired or congenital trochlear nerve palsy, Listing’s plane of the affected
eye does not rotate temporally upon convergence. This finding suggests an
important role of the SO in modifying the orientation of Listing’s plane as a
function of vergence [57]. In patients with acute trochlear nerve palsy, Listing’s
law is violated by the affected eye during downward saccades; this eye shows
dynamic extorsion as a result of the missing agonistic action of the SO [58]. In
patients with central abducens nerve palsy, Listing’s law is violated by both
eyes, while in patients with peripheral abducens nerve palsy, Listing’s law is
violated by the paretic eye and in the acute state only [59].
Compared to healthy subjects, patients with intermittent horizontal strabis-
mus exhibit a similar, but more variable relation between vergence angle and

angle between the Listing’s planes [60]. In patients with intermittent exotropia,
vertical gaze-dependent cyclovergence is increased, possibly because additional
convergence is required to cancel the exodeviation between the two eyes [61].