SensoryMotor deficits following neonatal binocular deprivation

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Sensory-Motor deficits following neonatal
binocular deprivation
Ronald G. Boothe Emory University Atlanta,
Georgia, USA
This presentation was a keynote address at the
Hospital for Sick Children 1st Eye Movement
Symposium A tribute to J. Raymond Buncic hosted
by the Department of Ophthalmology and Vision
Sciences at the University of Toronto on 20
September 2003.
(The text for this talk is on the Notes Pages)
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Sensory components of sensory-motor
Eyes Function as Components of Sensory-Motor
Systems

• Sensory Activities

• Photons of light from the environment are focused
  by the optics of the eye to form an image on the
  retina.
• Photoreceptors in the retina transduce light
  energy into neural signals that are transmitted
  to the visual processing portions of the central
  nervous system.
• Visual percepts such as form, motion, and color
  are produced from visual processing occurring in
  different brain regions.
• Percepts allow us to experience and interpret
  information about the outside world.

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Motor components of sensory-motor
Eyes Function as Components of Sensory-Motor
Systems
2. Motor Activities

• Eye stabilization eye movement systems help
  eliminate blur when the head moves.
• Fast eye movement systems facilitate rapid
  scanning of the environment.
• Fixation and smooth pursuit systems allow
  detailed vision by maintaining the image of an
  object of regard near the fovea.
• Coordination of the positions of the two separate
  eyes is a prerequisite for single binocular
  vision.

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Sensory-motor development

• Neither the Sensory nor the Motor systems are
  mature at birth.

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Normal Development of sensory (Teller)
Teller, 1997 ? Young
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Example of normal development stereopsis
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Example of normal development Binocular alignment
Boothe and Brown, 1996
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Sensory-Motor development requires postnatal
visual experience

• Neither the Sensory nor the Motor systems are
  mature at birth.
• Furthermore, both systems require binocular
  visual stimulation during the postnatal period in
  order to develop normally.

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Classic Visual Deprivation Syndrome

• 1. Described by Hubel Wiesel, and by von
  Noorden based on studies of visual deprivation in
  infant monkeys.
• These studies built on earlier work with other
  animals, primarily kittens.

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Classic Visual Deprivation Syndrome

• 2. Characteristic physiologic effects in visual
  cortex

• Loss of binocular cells.
• Shift of ocular dominance to untreated eye.

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Classic Visual Deprivation Syndrome

• 3. Characteristic anatomic changes.

• Ocular dominance columns for untreated eye expand
  at expense of deprived eye.
• Secondary effects seen in cell soma size in
  lateral geniculate nucleus.

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Classic Visual Deprivation Syndrome

• 4. Characteristic behavioral deficits.

• Poor binocular function (stereopsis).
• Loss of acuity in deprived eye.

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Classic Visual Deprivation Syndrome

• 5. General principles derived from these
  empirical studies with monkeys.

• There is a sensitive period of postnatal brain
  development during which visual input (what we
  see) influences what brain connections get made.
• Mechanism of monocular deprivation effects is
  binocular competition.

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Classic Visual Deprivation Syndrome

• Modern synthesis of Basic Neuroscience and
  Clincal Ophthalmology literatures

• Amblyopia is human analog of Visual Deprivation
  Syndrome seen in monkeys.
• Thus, we can study properties of amblyopia
  (including basic mechanisms of neuropathology,
  and causal relationships) by using the monkey
  model.

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The modern synthesis has a major problem that
was not usually addressed in the historical
literature on this topic.
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A number of motor deficits are commonly
associated with amblyopia in children (especially
amblyopia of neonatal onset)

• strabismus (esotropia or exotropia)
• dissociated vertical deviations (DVD)
• latent nystagmus
• asymmetrical eye movements in response to
  horizontal motion

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None of these motor deficits were described as
part of the Classic Visual Deprivation Syndrome
in Monkeys.Why not?

• The causal relationships between sensory and
  motor deficits were uncertain.

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Implicit Causal Relationships Assumed in the
Historical Literature
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Proposed Alternative Causal Relationships
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None of these motor deficits were described as
part of the Classic Visual Deprivation Syndrome
in Monkeys.Why not?

• The causal relationships between
  
• sensory and motor deficits were
• uncertain.

• Deprivation studies were often conducted by
  neuroscientists who did not look at behavior of
  monkeys.
• Most deprivation studies in monkeys did not start
  deprivation until 3 to 4 weeks after birth.

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Latent Nystagmus in the absence of visual
experience
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Strabismus and unstable gaze in absence of visual
experience
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Two Sensitive Periods

• 12 weeks / 1 year

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Alternating Monocular Occlusion (AMO) rearing
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Example of strabismus following AMO rearing
Target 10 cm to subjects left
Target directly in front of the subject
Target 10 cm to subjects right
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Quantitative assessment of strabismus in AMO4
RE
LE
RE
LE
RE
LE
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Cartoon illustrating incomitant strabismus in AMO4
24o
15o
30
0
10
15
25
20
5
-5
-10
-15
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Demonstration of disconjugacy in AMO4
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Disconjugacy results in incomitant strabismus at
end of pulse
Misalignment at end of Saccade in degs (RE-LE)
Orbital position of Right Eye (Degs)
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Disconjugacy results in incomitant strabismus in
steady state
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Gaze holding during fixation of steady target
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Nasal-temporal asymmetries during smooth pursuit
tracking
Lai Ngor Fu, Doctoral Dissertation, Emory
University, 2003
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Motion Asymmetries measured with VEPs
Wilson et al, 1999
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Motion Asymmetries measured psychophysically
Fu and Boothe, 2001
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Cortical and Subcortical neural processing systems

• Binoc processing system 1

Primary Visual Cortex
extrastriate Visual Cortex
Subcortical and oculomotor nuclei

• Binoc processing system 2

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First stab at constucting a Neural Model to
relate sensory and motor deficits
Fu and Boothe, 2001
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Collaborators
Yerkes/Emory
James Wilson Alcides Fernandes Vallabh Das
Michael Quick Cynthia ODell Rick Brown Lai Ngor
Fu Michael Goodman
Michael Mustari Ron Tusa
Washington University
Smith-Kettlewell
Larry Tychsen Andreas Burkhalter
Anthony Norcia Arthur Jampolsky