The Role of Cortical Attentional Systems in Eye Tracking Dysfunction

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The Role of Cortical Attentional Systems in Eye
Tracking Dysfunction

• Sam Hutton
• Department of Psychology
• University of Sussex

• What should we be trying to explain?
• Attention during pursuit maintenance

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What should we be trying to explain?
Hutton et al, 2001
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The effects of short and long term antipsychotic
medication on smooth pursuit gain
Hutton et al, 2001
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What should we be trying to explain?

• A small reduction in velocity gain.
• NO increase in CUS or AS compared to healthy
  controls (c.f. Sweeney et al, 1994).
• NO impairment in lag, suggesting some element of
  prediction is preserved.
• Severe impairment in chronic patients mediated by
  antipsychotic medication (c.f. Bartfai et al,
  1983 Kufferle et al, 1992).
• See also Sweeney et al, 1992 Friedman et al,
  1991 Malaspina et al, 1994.

• ANTIPSYCHOTIC MEDICATION IMPAIRS PURSUIT
• Pursuit mechanisms are sensitive to
  dopaminergic modulation
• Pursuit is impaired in PD patients
• Pursuit improves with l-dopa / apomorphine
  administration (e.g. Bares et al, 2003)

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Why cant people with schizophrenia track a
smoothly moving target?

• Hypotheses
• Saccadic disinhibition DLPFC / FEF.
• (Levin)
• Motion processing deficit V5 (MT/MST).
• (Chen / Holzman / Lencer)
• Extra-retinal deficit - velocity store /
  prediction / anticipation / efference copy
  working memory? DLPFC / FEF / PPC.
• (Barnes, Lencer, Thaker, Trillenberg / Heide).
• All of the above but all secondary to a more
  fundamental deficit in the ability to sustain and
  focus spatial attention DLPFC / FEF / PPC.

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A fundamental mechanism?
Smooth pursuit impairments are observed in
Patients with cerebellar and brainstem lesions,
lesions to most cortical areas, nigrostriatal
degeneration, corticobasal degeneration,
Alzheimers disease, Parkinsons disease,
Huntingtons disease, PSP and many other
neurological disorders. Smooth pursuit
impairments are also observed in Patients with
schizophrenia, depression, bipolar disorder,
autism, obsessive compulsive disorder, anorexia
nervosa and schizotypal personality
disorder. Poor smooth pursuit has been observed
in The young, the elderly, people with whiplash
injuries, people with tension headaches,
alcoholics and cocaine users. Same impairment in
all? Not enough data.
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Smooth Pursuit Attention

• Majority of studies have investigated role of
  attention during pursuit initiation
• Role of attention in steady state pursuit is less
  clear
• Enhancing attention to target improves pursuit in
  both schizophrenic patients and controls (Holzman
  et al, 1976 Shagass et al, 1976 Cegalis
  Sweeney, 1981 Sweeney et al, 1994 Schlenker et
  al, 1994)
• Effects of dividing attention are inconsistent
• Impairs (Acker Toone, 1978 Kaufman Abel,
  1986 Pass et al, 1978)
• Improves (van Gelder et al, 1995 Kathmann et al,
  1999)

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A role for cognitive processes in pursuit?
In contrast to saccades, pursuit is often
considered as a visual reflex - an automatic
process, that runs optimally in the absence of
top-down input (c.f. Kathmann et al
1999). Krauzlis (2004/5) has suggested that the
differences between the pursuit and saccadic
systems have been over-emphasised.
He argues that pursuit and saccades share much of
the same functional architecture This is an
important position as it suggests that top down
influences on pursuit may be greater than
generally assumed.
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Smooth Pursuit Attention

• Brezinova Kendell (1977) Smooth pursuit eye
  movements of schizophrenics and normal people
  under stress.
• Used EOG to measure pursuit in 10 controls under
  a variety of conditions, including threat of
  shock, serial subtraction and fatigue / boredom.
• Abnormal tracking patterns indistinguishable
  from those observed in schizophrenics can be
  produced in normal people by distracting them, or
  allowing their attention to wane through boredom
  or fatigue

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Smooth Pursuit Attention

• Early attentional accounts were quickly
  dismissed
• The difference between distracted and
  pathological smooth pursuit eye movement is the
  appearance of sporadic interruptions of smooth
  pursuit eye movements, in a setting of otherwise
  intact cycles of pursuit. Lipton et al, 1980.
• We believe it reasonable to infer that
  inattentiveness and disinterest in the task are
  not involved
• rather we would relate the dysfunction to a
  failure to maintain a visual-attentive focus that
  is continually locked onto the moving pendulum, a
  failure of cognitive centering, in spite of a
  desire to do the task. Holzman et al, 1976.

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A dual task study in controls
Smooth Pursuit performance was impaired by the
boustrophedon tapping pattern, but not by any of
the other secondary tasks. Limited resources for
internally representing spatial information?
Hutton Tegally, 2005
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Attention, schizophrenia and pursuit

• Does the abnormality in schizophrenia reflect
  abnormal attentional processes leading to a
  failure of centering?
• Participants pursue X and respond to sudden
  changes in colour occurring in the flankers
• O O O O X O O O O

In controls, attention appears focussed 1-2
degrees in front of the target. (c.f Van Donkelar
et al, 19992002) Performing a concurrent task
increases RT and results in a less specific focus
of attention High schizotypes show a slightly
less specific focus Data is currently being
collected on chronic schizophrenia patients.
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Low Frequency rTMS Study
Measured pursuit before and after stimulating PPC
(P4) or MC with 6 mins offline 1Hz rTMS. Order
counterbalanced across 18 participants.
Time x Position interaction significant - F(1,17)
5.2, p lt 0.05.
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Attentional correlates of pursuit function

• Surprisingly little evidence - most studies
  looking at cognitive correlates of pursuit
  dysfunction have small Ns and / or limited range
  of measures of attention.
• In our large (N109) FE sample Spatial Span
  (just)
• No correlation with AS in our study not
  necessarily both indicators of same underlying
  impairment
• Ross et al (1998) sensory integration
  scores worse in poor eye trackers.
• Sensory integration Audio-visual integration,
  Stereognosis, graphesthesia and left / right
  confusion.
• All require the ability to internally represent /
  manipulate spatial information

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Conclusions

• Smooth pursuit impairments at first episode are
  mild, and severe impairments are limited to a
  very small sub-group of patients.
• Impairments in motion perception / prediction /
  anticipation / inhibition of intrusive saccades
  may all contribute to pursuit dysfunction in
  schizophrenia.
• All of these impairments may be secondary to a
  more fundamental impairment in the ability to
  focus and sustain spatial attention on the
  pursuit target / generate an accurate internal
  representation of its motion.
• Given the sensitivity of the pursuit system it
  will be critical to establish whether there are
  any pursuit abnormalities that are truly specific
  to patients with schizophrenia.

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What should we be trying to explain?

• Some people with schizophrenia have mild
  impairments in smooth pursuit eye movements
• So do some people with many other psychiatric
  disorders
• So do most people with many different
  neurological disorders
• So do children and so do old people.
• 84 of first-episode schizophrenia patients hear
  voices
• 81 have persecutory delusions
• If we want to understand anything about
  schizophrenia, this is what we should be trying
  to explain.

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The Dodge Photochronograph
Used a tuning fork to operate a shutter at
100Hz Slowly falling photographic plate to record
corneal reflection
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• Saccadic eye movements normal
• Pursuit tracking impaired

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Why study eye tracking in Schizophrenia?

• Smooth pursuit abnormalities are well documented
  in schizophrenic patients and their first degree
  relatives and are therefore considered a valuable
  biological marker for genetic vulnerability to
  the illness.
• (Endophenotype approach).
• Our understanding of the neural systems involved
  in oculomotor control is reasonably advanced and
  distinctive abnormalities of ocular motility may
  provide important clues to a specific
  pathophysiology, anatomical localisation, or
  pharmacological disturbance.
• (Neuroscience approach)

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• What is attention?
• Ask 100 psychologists get 100 answers.
• The ability to selectively process a subset
  of the total amount of information available
• Top down biases in info processing
• Spatial Attention
• Visual world represented in various
  topographic maps throughout cortex (occipital /
  parietal frontal?) sub-cortex (e.g SC) and
  cerebellum.
• Goals / intentions (frontally mediated) bias
  specific areas in these maps

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Need slide at beginning outlining a rough model
of attention e.g. that it emerges as a result
of frontally mediated biases in info processing
PPC maintains representations of external
space in codes appropriate for motor output
these representations are modulated by
attention.Motion information as well as
spatial information can be represented, although
the representations of spatial information appear
to be far more robustThese maps are repeated in
various forms throughout the brain (e.g. SC as in
Krauzlis) there is some kind of fundamental
problem in Sz that may exist at the highest level
(and feed down) or may exist at all
levels.Attention is an emergent
property?Attention emerges due to biases (top
down) mediated by prefrontal cortex areas these
highten activity in particular regions of the
maps?Need to accommodate Lencers 2004 psych med
finding that velocity post-saccades is reduced
in Sz could this be attention? E.g.
reacquisition of target
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Different kinds of learning / expectation
different kinds of models? Which is impaired in
schizophrenia both?Target blanking data
speaks to the very short term one, but what about
the longer term?Discrepancies wrt SZ pursuit of
unpredictable targets if less reliant than
controls on extraretinal signals the impairments
should be less. There is no evidence for
this.Reason Lencer find V5 and not frontal is
cos they compare to fixation fixation will
activate frontal massively.Further evidence for
general failure of top down modulation of visual
processes comes from Malaspina 2004 figure /
ground problems in Sz.Friedman et al, 1991
correlation of 0.8 between days on medication and
pursuit gain!!! (N6)!(Bares et al, 2003)
conclude that the dopaminergic improvement is
caused by a more general influence, as for
instance an increase of arousal level and
attention). ADHD? (c.f. bylsma pivik, 1989)
but not in Ross paper - but ADHD are not sig diff
from patients on several measures power a big
problem. Attentional dysfunction is probably
milder in ADHD than in schizophrenia!!!
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What brain damage leads to pursuit deficits in
non-schizophrenic patients?

• Requires a detailed understanding of exactly how
  pursuit is dysfunctional in schizophrenia
• Until recently pursuit measurements in patients
  with schizophrenia were very crude.
• Best way to measure pursuit performance is still
  debated
• Recent research suggests pursuit deficits in Sz
  are best characterised by a reduction in velocity
  gain and an increase in corrective catch up
  saccades.
• Damage to almost all cortical areas can result in
  smooth pursuit dysfunction characterised in this
  way (Lekwuwa Barnes, 1998).
• Pharmacology of pursuit not clear, but
  Parkinsons patients are impaired (and improve
  with l-dopa).

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What other indices of neuropathology correlate
with pursuit deficits in patients with
schizophrenia?

• No relationship between pursuit and change in
  ventricular volume over 1 Year (N28)
• No relationship between SP performance and
  movement disorders, either at baseline or 1 year
  (Ngt100)
• No relationship between SP performance and any
  measure of symptom severity at baseline (Ngt100)
• No correlations between pursuit and any
  neuropsychological measure (Hutton et al 2004).