Download Smooth Pursuit Impairment in Schizophrenia— What Does It Mean?

37
VOL 9, NO. 1, 1983
Smooth Pursuit
Impairment in
Schizophrenia—
What Does It
Mean?
Abstract
The significance and nature of
smooth pursuit impairments in schizophrenia are considered. Studies of
potential artifacts show that the phenomenon is not due to medications,
age, inattention, or poor motivation.
Abnormal pursuit eye movements in
schizophrenics consist of intrusive
saccades which are present during
any visually guided slow r •. t movements, and in some patients are related to nonvoluntary attention. These
results rule out a generalized motor
or oculumotor dysfunction, as well
as a specific pursuit system dysfunction. The findings are consistent with
a cortical dysfunction which results
in saccadlc disinhibition. Questions
are raised for future research.
The first question to be considered is
whether the phenomenon of smooth
pursuit impairment may be an artifact. Is it merely a drug effect? Is it
related to subjects' age? Does it represent simple lack of interest in the
tracking task? The data relating to
these and other questions will be
briefly summarized here. A more detailed review can be found in Lipton
et al. (this issue). The nature of
smooth pursuit impairment will also
be discussed, and some hypotheses
about the underlying dysfunction and
its localization will be raised.
Drug Effects
The earliest reports of smooth pursuit impairment in psychiatric patients were made before the era of
antipsychotic medications (Diefendorf and Dodge 1908; Couch and
Fox 1934; White 1938). There can be
little doubt, then, that eye tracking
dysfunction (ETD) is not merely a
motor side effect of neuroleptic or
other antipsychotic medications. Later studies found no differences between medicated and unmedicated
patients (Holzman et al. 1974;
Shagass, Roemer, and Amadeo 1974;
Karson 1979), or between patients'
performance off and on medication
(Spohn 1981). Quality of pursuit remains stable, in repeated measurements, in spite of changes in clinical
state related to drug treatment (Levy,
Lipton, and Holzman 1982). Furthermore, first-degree relatives who
themselves were not ill and were not
being treated pharmacologically
showed the same kind of ETD as did
patients (Holzman et al. 1974; Kuechenmeister et al. 1977; Holzman et
al. 1978, 1980). Thus the available
evidence suggests that ETD is not an
artifact of antipsychotic medication.
Age Effects
Smooth pursuit is an age-dependent
motor system (Sharpe and Sylvester
1978). Young adult subjects, whether
healthy or psychiatrically affected,
are better trackers than subjects over
50 years old (Shagass, Roemer, and
Amadeo 1974; Holzman and Levy
1977; Kuechenmeister et al. 1977;
Spooner, Sakala, and Baloh 1980), or
children under 13 (Miller, Arboleda,
and Holzman 1982). This raises the
possibility that age accounts for the
prevalence of ETD in psychiatric
populations, particularly in those
found in long-term custodial hospitals. Holzman and Levy (1977) reported, however, that age accounted
for only 15 percent of the variance of
a quantitative measure of ETD. Furthermore, ETD in a sample of young
recent-break schizophrenics (mean
age — 23 years, SD = 4) was significantly greater than in age-matched
normal controls (Lipton, Levin, and
Holzman 1980). ETD was also not
related to age in groups of identical
SCHIZOPHRENIA BULLETIN
38
twins discordant for schizophrenia
(Holzman et al. 1978, 1980). Thus,
although studies of eye movement
function must control for age, the
phenomenon of smooth pursuit impairment in psychiatric patients is
not an artifact of age.
Demographic Background and
Chronicity
Holzman et al. (1974) first reported
that ETD was more prevalent in a
state hospital sample of chronic
schizophrenic patients than in patients from a private psychiatric institution. Up to 85 percent of schizophrenic patients had ETD in a state
hospital, whereas only 50 percent did
in a private psychiatric institution.
Similar rates, respectively, were reported by Lipton, Levin, and Holzman (1980) for another private hospital, and by Latham et al. (1981) for a
state facility. Two likely explanations
for these findings must be considered. The sample differences may be
related to idiosyncratic characteristics
of different hospitals. Alternatively,
they may reflect spurious correlations
between the type of hospital and
sample characteristics such as chronicity and socioeconomic status
(SES). The first explanation is weakened by the similarity between types
of hospitals across studies. The fact
that findings of ETD have now been
replicated in more than a dozen samples across the world (see review in
Lipton et al., this issue) also provides
a reasonable control for hospitalization variables.
The second explanation is less easily dismissed. The structure of psychiatric services is such that the majority of patients in private psychiatric hospitals have a high enough SES
to afford medical insurance; even
these patients are generally recentbreak or ambulatory patients who
have not exhausted their medical
coverage resources. In contrast, patients in state hospitals have lower
SES and have been sick most of their
lives. SES is related to social, psychological, and organismic competence, and therefore also to illnessspecific variables such as chronicity
and severity. Thus, sample differences in the prevalence of ETD may
not be trivial artifacts, but rather
provide meaningful inroads to further the study of etiological heterogeneity in schizophrenia.
Attention
Schizophrenic patients are emotionally and socially withdrawn; they are
frequently lost in a world of delusions and hallucinations. It has been
suggested that ETD is merely a reflection of these patients' inattention
and lack of involvement in the tracking task (Couch and Fox 1934; Brezinova and Kendell 1977). Brezinova
and Kendell (1977) studied the effects
of stress, fatigue, and distraction in
normal subjects and reported that
distraction produced ETD. They concluded that ETD in schizophrenia
was due to distraction. Acker and
Toone (1978) also reported that pursuit in normal subjects deteriorated
as a function of the degree of difficulty of a distracting task, and that
among patients, anxious schizophrenics had the worst tracking.
Holzman, Levy, and Proctor
(1978) followed William James (1950)
and Kraepelin (1919) in distinguishing between involuntary or passive
attention and voluntary or active attention. They suggested that ETD in
schizophrenia was related to a dysfunction of passive, involuntary attention and not to lack of motivation
or inattentiveness. This conclusion
was based on several findings. Verbal alerting instructions have no effect on the quality of pursuit, al-
though patients who have stopped
tracking do return to the task (Holzman, Proctor, and Hughes 1973;
Shagass, Roemer, and Amadeo 1974;
Pivik 1979a). Stronger motivational
manipulations, such as giving patients cigarettes or money for good
performance, are similarly ineffective
in improving tracking (May 1979).
The findings that saccadic eye movements of schizophrenic patients are
normal, and particularly saccadic reaction times, further weaken the
proposition that ETD is an artifact of
inattention (Diefendorf and Dodge
1908; lacono, Tuason, and Johnson
1981; Levin, Lipton, and Holzman
1981; Levin et al., 1982b). Moreover,
with respect to the finding of Brezinova and Kendell (1977), it is of interest that stress, fatigue, or moderate distraction did not impair tracking. Smooth pursuit in this study was
only impaired when subjects had to
do a difficult mental calculation (serially subtracting 13 from 200) and
write down the result while following
a moving target. Lipton, Frost, and
Holzman (1980) showed that even
this complex task, itself requiring eye
movements, disrupts normal pursuit
in a manner that can be reliably distinguished from ETD of schizophrenic patients. Distraction by competing
tasks also did not affect schizophrenics' tracking compared to their baseline (Pass et al. 1978). Taken together, these findings suggest that
mere lack of motivation or inattentiveness, while possibly affecting the
subject's ability to track at all, does
not produce the characteristic ETD in
schizophrenia.
Nonvoluntary attention, or the
ability to center on and grasp the target, may be involved, however, in
ETD in schizophrenia. Tasks which
introduce unpredictable changes in
the target—changing numbers,
changing colors, intermittent second
39
VOL.9, NO. 1, 1983
target, or interruptions in tracking
light—evoke optimal levels of visual
centering (e.g., Holzman, Levy, and
Proctor 1976; Shagass, Amadeo, and
Overton 1976; Pivik 1979a). Patients
are not aware that their tracking improves, or that it deteriorates again
as soon as the attentional task is removed, suggesting that the effect is
mediated by a nonvoluntary process.
Furthermore, since attentional manipulations also improve ETD caused by
central nervous system depressants,
such as alcohol and barbiturates,
ETD is not primarily related to poor
motivation and inattention (Levy,
Lipton, and Holzman 1981).
A further clue about the role of
nonvoluntary attention in ETD is
provided by the finding of two basic
types of smooth pursuit impairment
(Holzman, Levy, and Proctor 1978).
Type I tracking consists of pursuit
that is almost completely replaced by
large irregular saccades, whereas in
type II, small amplitude saccades are
superimposed on smooth pursuit
tracking and give it a "spiky" or cogwheeled appearance. Type I tracking
tends to normalize with an attentional task, suggesting that it is related to
a dysfunction of nonvoluntary attention. In contrast, type II tracking is
relatively unaffected by attentional
tasks. This suggests that in a subgroup of poor trackers ETD is not directly related to a dysfunction of attentional focus or "auffassung"
(Holzman, Levy, and Proctor 1978).
The fact that in type I trackers ETD
reappears as soon as the attentional
task is removed indicates that, even
in these patients, ETD is related to a
central nervous system (CNS) disorder which the attentional tasks may
only temporarily circumvent or override.
In conclusion the available evidence suggests that ETD in schizophrenia is not an artifact of poor mo-
tivation, inattention, or other aspects
of voluntary attention. The ameliorative effect of attention-enhancing
tasks on ETD in some patients indicates, however, that nonvoluntary
attention may be involved in the pursuit impairment, although it is not
the primary underlying dysfunction.
Rather, the data suggest that ETD in
the functional psychoses is closely related to a physiological, CNS dysfunction. The following section will
review the nature of this dysfunction.
Characterization of ETD in
Schizophrenia
There are three basic types of versional eye movements: smooth pursuit, saccades, and vestibulo-ocular
reflex (VOR) movements. To define
and characterize the nature of ETD in
schizophrenic patients, it is useful to
examine these versional eye movements under a variety of tracking
conditions. Since smooth pursuit,
saccades, and VOR movements are
controlled in different parts of the
brain, a comparison of these different
eye movement systems can provide
clues about both the nature of the
dysfunction and its possible localization.
Types of Impaired Eye Movements.
With respect to the type of versional
eye movement that is affected in
schizophrenia, Levy, Holzman, and
Proctor (1978) and Latham et al.
(1981) found a dissociation between
vestibular and visual eye movement
control. Levy, Holzman, and Proctor
(1978) used caloric stimulation to induce nystagmus eye movements, and
reported that nystagmus response in
schizophrenic patients was essentially
normal. Latham et al. (1981) tested
optokinetic nystagmus (OKN) under
two types of conditions, a full-field
stimulus which is thought to stimu-
late a subcortical vestibular pathway,
and a partial-field stimulus which is
considered identical to visual pursuit
with refixation saccades. Latham et
al. (1981) found that schizophrenic
patients who had smooth pursuit
dysfunction also had impaired partial-field OKN, but their full-field
OKN was intact.
Several studies examined tracking
under different tracking conditions.
Lipton, Levin, and Holzman (1980)
first reported that when schizophrenic patients generate slow eye movements via the vestibulo-ocular reflex—by fixing their eyes on a stationary target while rotating their
head—these eye movements are quite
smooth and free of intruding saccades. The same patients had smooth
pursuit impairment when tracking a
moving target. Levin et al. (1982a)
confirmed this finding and further
showed that compensatory VORs
made while refixating a target with
both head and eyes (head-eye saccades) also appeared normal and
were free of saccades. In contrast, in
patients tracking a moving target
with both head and eyes (head-eye
pursuit), pursuit eye movements were
impaired by saccadic intrusions as
they were with the head restrained.
These findings suggest that generation of slow eye movements is adequate when it is based on vestibular
signals but not when it is based on
visual signals.
These nystagmus and VOR findings have several functional and anatomical implications. First, they suggest that ETD in schizophrenia does
not affect all eye movements, and
not even all slow eye movements,
but is restricted to slow pursuit of
visual targets. Second, they suggest
that the midbrain and brainstem
mechanisms for control of VOR
movements are intact in schizophrenia. These include the motor system
SCHIZOPHRENIA BULLETIN
40
of eye movement control, which receives the direct vestibular-nudear
projection in the VOR arc, and the
vestibulocerebellum (the flocculonodule), which receives ascending vestibular-apparatus fibers (Cohen 1971,
1974). Since smooth pursuit control
converges with the vestibular pathways at both the premotor cerebellar
and oculomotor levels, the nystagmus and VOR findings argue against
an involvement of these areas in pursuit impairment.
Although the vestibular findings
indicate that a lower motor pathway
or a cerebellar dysfunction is unlikely, they do not address the possibility that ETD may be localized at the
horizontal gaze center, in the paramedian pontine reticular formation
(PPRF). This hypothesis is weakened
by several findings that saccadic eye
movements, whose subcortical control center converges with horizontal
pursuit at the PPRF, are intact (Diefendorf and Dodge 1908; Iacono,
Tuason, and Johnson 1981; Levin et
al. 1981, 1982b). Visually guided saccades of schizophrenic patients who
have smooth pursuit impairment
have normal saccadic latencies (Diefendorf and Dodge, 1908; Iacono,
Tuason, and Johnson 1981; Levin et
al. 1981), and normal trajectories
(Levin et al., 1982b). Furthermore,
their dynamic characteristics—the relationships between the speed and
duration of the eye movements, and
their size—were the same as those
seen in normal subjects (Levin et al.
1981, 1982b).
In sum, the evidence for clear dissociations between pursuit impairment on the one hand and vestibuloocular and saccadic functions on the
other suggests that ETD in schizophrenia is not related to a brainstem
dysfunction. Furthermore, these findings argue against the hypothesis that
pursuit impairment reflects a general-
ized oculomotor dysfunction, or a
dysfunction of slow eye movements
in general. A generalized motor slowing is also ruled out by these findings, as well as by data showing that
schizophrenics have normal visual
but slowed hand reaction times
(Iacono, Tuason, and Johnson 1981;
Levin et al. 1981). Finally, the dissociation between pursuit and saccades,
and the finding of impaired cortical
OKN, both suggest that ETD in
schizophrenia may be related to a
cortical dysfunction.
Precis* Pattern of Impairment. With
respect to the precise pattern of ETD
in schizophrenia, Diefendorf and
Dodge (1908) showed photographic
records of smooth pursuit eye movements which were disrupted by saccades. They called this pattern "stepping." A recent study using highresolution reflected light recording
techniques showed that smooth pursuit impairments in schizophrenic patients consist of saccadic intrusions
and saccadic smooth pursuit tracking
(Levin et al. 1982a). Saccadic intrusions are small back-to-back saccades
that are superimposed on smooth
pursuit; they are also seen in normal
subjects (Bahill, Clark, and Stark
1975; Herishanu and Sharpe 1981),
as well as in people with dyslexia
(Adler-Grinberg and Stark 1978),
strabismus amblyopia (Ciuffreda,
Kenyon, and Stark 1979a, 1979b),
and cerebellar disease (Selhorst et al.
1976). Saccadic smooth pursuit tracking consists of small saccadic steps,
which intermittently or continuously
replace smooth pursuit tracking and
are similar to the "staircase" tracking
in patients with cerebellar atrophy
(Baloh, Konrad, and Honrubia 1975).
Both these types of saccadic interruptions coexist in pursuit eye movements of individual patients, and appear to correspond to type II tracking
(Holzman, Levy, and Proctor 1978).
Although several other studies reported that ETD in schizophrenia
consists of saccadic interruptions of
pursuit, these reports were put in
question by studies showing discrepancies between eye movement records obtained with electro-oculographic (EOG) and infrared (IR) recording techniques (LJndsey et al.
1978; Iacono and Lykken 1981). The
findings by Levin et al. (1982a) show
unambiguously that smooth pursuit
in some schizophrenic patients is in
fact disrupted by saccadic intrusions.
Since clear recordings of these eye
movements require a recording system with a frequency response bandwidth of DC to 150 Hz, it may be
possible that the IR recordings reported by both Lindsey et al. (1978)
and Iacono and Lykken (1981) did
not represent their data accurately,
since they were traced by a polygraph with a slow pen and a lower
high-frequency cutoff. This does not
rule out, however, the possibility
that EOG recordings reflect, in addition to smoothed out tracings of saccades, evidence for other bioelectric
signals picked up by the skin-surface
electrodes (Iacono and Lykken, this
issue).
The presence of saccadic intrusions
and saccadic smooth pursuit tracking
further clarifies the process that may
underlie ETD in schizophrenia. Holzman, Levy, and Proctor (1978) suggested that smooth pursuit impairment may reflect a disinhibition of
saccades during pursuit tracking, and
related this dysfunction to other disinhibitory phenomena in psychopathology, such as sensory proprioceptive
disorders (Holzman 1969) and
thought disorder (Holzman 1978).
This interpretation is consistent with
the dual-mode control of visual
tracking, whereby tracking is accomplished by both the saccadic and
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VOL 9, NO. 1, 1983
smooth pursuit control systems
working independently but in concert, with inhibitory feedback regulation (Rashbass 1961; Stark 1971).
Such feedback mechanisms ensure
that saccades will be inhibited as
long as smooth pursuit is accurate
and efficient. They are disinhibited
when target position errors occur—
for example, when pursuit becomes
sluggish, when pursuit gain is too
high, and when target velocity
changes suddenly or exceeds the velocity capacity of the pursuit system.
Saccadic eye movements may also interrupt smooth pursuit when other
visual targets of interest compete for
the tracker's attention. Thus normal
smooth pursuit depends on the presence of a slowly moving visual target, on the ability of the smooth pursuit system to follow the target with
appropriate speed, and on the ability
of the saccadic system to remain silent except when position errors occur.
According to the model of dualmode control of visual tracking, ETD
in schizophrenia may be due to the
following conditions: (1) Schizophrenic patients suffer from an attentional dysfunction which impairs
their ability to focus on the moving
target; consequently they make extraneous saccadic movements in the direction of distracting peripheral targets. (2) The pursuit system is inefficient in schizophrenia, with the result
that pursuit velocity and gain do not
match the target, generating position
errors that require corrective saccades. (3) The feedback mechanisms
whose function is to inhibit saccades
during dual-mode control of pursuit
are dysfunctional, so that unnecessary saccades are made during tracking.
The data reviewed above suggest
that for some schizophrenic patients—those with saccadic intrusions
and type II tracking—the first hypothesis is not very likely. As previously mentioned, attentional tasks
that aid attentional focus on the target did not improve tracking for type
II trackers. The fact that saccadic intrusions are regular and small in size
(.5-2.5 degrees of visual arc) suggests
that they are not used to scan the
visual periphery for distracting targets. The data do suggest, however,
that another subgroup of schizophrenic patients—those with type I
tracking—may in fact have an impaired ability to focus on the tracking target, and a predilection for distractibility by peripheral stimuli.
The second hypothesis, of a specific pursuit dysfunction, has not been
examined directly, although some
converging evidence renders it unlikely. First, several studies reported
no significant effect of target frequency on ETD in schizophrenia,
suggesting that schizophrenic patients' pursuit mechanisms for velocity matching are comparable to those
of normal subjects (Kuechenmeister
et al. 1977; Cegalis and Sweeney
1979; May 1979; Pivik 1979fe; Levin,
Lipton, and Holzman 1981). Second,
visual inspection and frequency analyses of tracking records suggest that
there is no relationship between saccadic intrusions and the phase of a
tracking cycle, indicating that changes in target velocity do not affect the
pursuit system (Bird, Levin, and
Holzman 1982). Most important, saccadic intrusions appear not only during smooth pursuit, but also during
fixation of a stationary target, suggesting that saccadic intrusions are
not related to target movement, but
to any condition of continuous visual
tracking (Levin et al., 1982a). Taken
together, these findings weaken an
explanation positing a specific dysfunction of pursuit eye movements,
although direct measurements of pur-
suit velocity and gain in schizophrenic patients remain to be conducted.
At the same time, the findings of saccadic intrusions and smooth pursuit
tracking support the hypothesis of
disinhibition of saccades. Since there
is considerable evidence for the role
of suprabulbar mechanisms in attention and eye movements, and particularly in disinhibition of saccades
(e.g., Goldberg and Bushnell 1981;
see review in Levin 1982), this argument is consistent with the proposition that ETD in schizophrenia reflects a cortical brain dysfunction.
Conclusion
Available studies of the nature of
ETD in schizophrenia show that the
phenomenon is not an artifact of antipsychotic drugs, age, inattention, or
poor motivation. Other incidental artifacts such as length of hospitalization or SES are of relevance only inasmuch as they are related to the
etiology and severity of the schizophrenic illness. Studies comparing
ETD under a variety of tracking conditions show that ETD is not a generalized motor or oculomotor dysfunction, and that it is specific to conditions which require continuous visual
tracking. The precise characterization
of saccadic intrusions during pursuit
and fixation eye movements renders
a specific dysfunction of the pursuit
system unlikely, and supports a hypothesis of a cortical dysfunction
that results in saccadic disinhibition.
The dissociation of pursuit dysfunction from vestibulo-ocular or saccadic movements also suggests a cortical localization for this eye tracking
dysfunction in schizophrenia.
Several open questions, however,
invite future research. For example,
the evidence for two types of tracking in schizophrenic patients, type I
42
and type II, raises the possibility that
more than one underlying process
may be responsible for ETD in
schizophrenia. Since schizophrenia is
most likely heterogeneous, it is useful
to explore the relationship between
ETD patterns and other behavioral
and biological phenomena which
may distinguish between subgroups
of patients. Another question worthy
of further study concerns the role of
attention in schizophrenics' ETD,
particularly with respect to other attentional and information processing
dysfunctions. For example, is the
process underlying long manual reaction times similar to that responsible
for disrupted pursuit? If so, what is
the process underlying visual reaction
times? Future work on these and
other questions will further our understanding of the nature of eye
tracking dysfunctions in schizophrenia.
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The Assessment
of Smooth
Tracking
Dysfunction
Abstract
The two main techniques for recording eye movements, electro-oculography (EOG) and infrared reflection
(IR), are discussed and compared.
Methods of quantifying eye movement dysfunction are also reviewed
and contrasted. It is concluded that
EOG and IR recordings both contain
information not present in the other
and that both methods will continue
to be useful. Similarly, although the
root-mean-square (RMS) and the signal-to-noise ratio (S/N) indices are
algebraic functions of one another,
the function is not linear and one or
the other may be more appropriate
to a particular application.
Recording Techniques
There are two readily available and
popular techniques for measuring eye
movements: electro-oculography and
infrared reflection. Comprehensive
reviews of both recording methods
can be found in a variety of sources
(Shackel 1967; Tursky 1974; Young
and Sheena 1975; Haines 1980; Oster
and Stern 1980).
Recording of the electro-oculogram
(EOG) is possible because a standing
potential of about 1 mV exists between the cornea and fundus of the
eye. When the eyes move, the volt-
Smadar Levin, Ph.D.
Mailman Research Center
McLean Hospital
115 Mill St.
Belmont, MA 20178
age differences generated by shifts in
the position of the two globes can be
monitored from periorbital electrodes. Horizontal eye movements
are usually recorded binocularly
from electrodes at the lateral canthi.
Monocular recording is also possible,
but tends to be less reliable and more
subject to artifact than measurements
taken across both eyes. Vertical motion is generally monitored monocularly from electrodes at superior and
inferior orbital rim placements and is
often used to detect eye blinks.
For infrared (IR) reflection, an IR
light source is positioned slightly below the center of one eye and within
several millimeters of the globe. Photodiodes which monitor reflected
light from the eye are positioned on
either side of the IR source. With this
method, the position of the limbus is
tracked. Since the sclera has greater
reflectivity than the iris and the
boundary between the two is relatively sharp, the ratio of reflected
light to the sensors on either side of
the limbus provides an accurate
measure of eye movement. Placement
of the light source and photodetectors is critical to obtain a good recording with this technique. Therefore, head position must be fixed in
some way, or the IR apparatus must
be mounted on goggles or frames
that are securely attached to the subject's head. It is worth noting that ex-