Are We Paying Attention Yet?

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Are We Paying Attention Yet?

• A review of the relation between attention and
  saccades
• By Travis McKinney

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Overview

• Corbetta Covert vs. Overt Orienting -gt fMRI and
  PET
• Moore and Armstrong FEF stimulation-gt V4
  response activity
• Moore and Armstrong FEF Stimulation -gt V4
  discriminability similar to attention effects

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Corbetta What is attention?

• Attention the mental ability to select stimuli,
  responses, memories, or thoughts that are
  behaviorally relevant among those that are
  irrelevant
• How does this relate to foveated vision?

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Overt Visual Orienting

• Exploring scenes by means of saccadic eye
  movements to bring the fovea onto the stimuli of
  interest
• Stimuli are processed during fixations
  interspersed between saccades

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Covert Visual Orienting

• Attending to behaviorally relevant stimuli in the
  absence of exploratory saccadic eye movements
• The locus of attention is dissociated from eye
  fixation
• Directing attention toward a location either
  voluntarily or reflexively when a stimulus
  abruptly appears in the visual field.

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Hypotheses for Attention/Eye Movement Relation

• Independence Attention and eye movement
  processes involve entirely different mechanisms
• Interdependence Attention and eye movement
  processes share resources or computations at some
  stage
• Identity Attention and eye movement processes
  involve the same mechanisms

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Current View

• Attention and eye movements are tightly related
• During saccade preparation, oculomotor system
  controls location selection even if attention is
  directed elsewhere
• Direction of attention is dissociable from eye
  position during fixations
• Findings are do not rule out interdependence or
  identity hypotheses
• Most findings oppose independence hypothesis

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Paradigm

• Shifting-attention task subjects asked to
  voluntarily shift attention along a series of
  locations positioned in left or right visual
  field to detect brief visual stimuli with speeded
  key-press response
• Shifting-attention task involves endogenous
  cueing and stimuli at attended locations were
  detected faster than at unattended locations
• Central-detection task subjects attended to and
  manually responded to stimuli in fovea while
  being presented with the same series of
  peripheral stimuli as in the shifting-attention
  task
• Areas involving covert orienting were localized
  by subtracting PET activity recorded during the
  shifting-attention task from activity recorded
  during central-detection task

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Shifting Attention Brain Data

• Shows differential activity between shifting
  attention task and central detection task (should
  show activity attributed to attention/covert
  orienting)
• Significant blood flow changes in superior
  parietal and frontal cortex
• Stronger activation in hemisphere contralateral
  to attended field

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Comparison between studies

• Exogenous cueing Yellow Foci
• Endogenous cueing Red Foci
• Parietal and Frontal regions coactivate when
  locations are cued exogenously and endogenously

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Overlap in Activation

• There is a very strong overlap in cortical
  activation patterns for spatial cueing and tonic
  attention
• Right hemisphere activity localizes along
  postcentral and intraparietal sulcus
• Left hemisphere activity straddles across
  postcentral and intraparietal sulcus
• Similarity in activation for tonic and
  shifting-attention supports idea that a
  frontoparietal network is the source of a
  selective location signal, not the site of
  attentional modulation

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Oculomotor System

• In the frontal lobe, activity centers onto
  precentral gyrus
• A second cluster of activity appears at posterior
  tip of superior frontal sulcus
• In the parietal cortex activity is distributed
  near intraparietal and postcentral culcus and
  adjacent gyri and extends towards the precuneus

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Brain Activity Attention vs. Saccades

• Eye movement activity evident dorsally in the
  right precuneus and left postcentral gyrus
• Attention activity evident ventrally in the
  intraparietal sulcus

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Brain Activity Attention vs. Saccades

• All three major sites of activation for attention
  (intraparietal, postcentral, and precentral) show
  convergent activation during eye movement
• Presence of attentional activity in frontal eye
  fields indicates that attention related signals
  can be recorded in an area strongly implicated in
  voluntary oculomotor planning
• This data supports the interdependence hypothesis
  and does not rule out the identity hypothesis
• This data does NOT support the independence
  hypothesis

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Attention vs. Saccades in same Subject

• Single subject scanned during covert
  shifting-attention task and during an overt
  shifting task
• Left and right visual field were tested
  independently
• Attentional activation and saccadic eye movement
  activation localized to identical brain regions
  for both left and right visual fields

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Monkey Studies Covert Orienting

• During tasks emphasizing exogenous cueing at a
  location a suppressive type of modulation has
  been found
• Neurons in parietal cortex gave a brisk response
  to a cue when flashed in visual field
• Responses to subsequently presented probe stimuli
  at attended locations were either
• Unaffected by cue 48
• Depressed by the cue 42
• Enhanced by the cue 10
• This suggests that the sensitivity of parietal
  neurons decrement at a given location after that
  location has been selected

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Monkey Studies Overt Orienting

• Oculomotor signals have been measured in many
  areas of the macaque brain (FEF, dorsolateral
  prefrontal cortex, caudate and superficial layers
  of superior colliculus, etc.)
• The neural response to visual stimuli is enhanced
  when the stimulus is the target of a saccadic eye
  movement
• Neurons in area LIP respond to visual stimuli and
  show preparatory oculomotor activity, indicating
  that attention and eye movement signals are
  tightly related at the neuronal level

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Monkey Studies Overt Orienting

• Monkeys trained in a spatially cued oculomotor
  task
• Saccadic reaction times for cued locations were
  faster than uncued locations for exogenous and
  endogenous cueing
• Electrical stimulation with microcurrents
  produced a displacement of the constant saccade
  vector in the direction of the cued location
• Normally, this stimulation would generate a
  saccadic eye movement of constant direction and
  amplitude
• Therefore attentional shifts independent of eye
  movements still lead to modification of evoked
  saccades

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Moore Armstrong Nature 2003

• Examined interaction between saccade preparation
  and visual coding with microstimulation of
  frontal eye fields
• Measured effect of microstimulation on neural
  activity in extrastriate visual cortex
• Microstimulation was below the level necessary to
  evoke a saccadic movement

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FEF Microstimulation

• FEF is involved in the selection of visual
  targets for saccades
• Electrical stimulation of FEF evokes
  short-latency saccades in human and non-human
  primates
• Stimulation below threshold does not evoke
  saccades, but biases the selection of eye
  movements and can improve a monkeys ability to
  covertly filter visual stimuli

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FEF Microstimulation

• Stimulation applied 200-500 ms after appearance
  of visual stimuli
• Neuron responds to stimulus in RF, but adapts
  within 250 ms
• Microstimulation enhanced response with respect
  to control condition (figure 2a)
• Microstimulation had no effect when no stimulus
  was present in RF (figure 2b)

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FEF Microstimulation

• When a stimulus is presented in RF,
  microstimulation enhanced V4 responses (figure
  3a)
• When no stimulus is present in RF,
  microstimulation has no effect on V4 population
  response (figure 3a)
• The preferred stimulus yields a greater response
  enhancement than the non-preferred stimulus
• The largest response enhancement occurs when the
  preferred stimulus is presented in the RF with a
  distractor outside the RF (figure 3b)

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Not always enhanced?

• V4 response suppression occurred when preferred
  stimulus was presented in the RF and a distractor
  was presented outside of the RF in cases when
  evoked saccade would not have been in direction
  of RF (figure 3b)
• FEF microstimulation appears to have activated a
  network that controls gain of visually driven
  signals
• Results show that activation of this network
  biases eye movement selection as well as strength
  of visual cortical signals, revealing a common
  network for visual and oculomotor selection
  (supporting identity or interdependence
  hypotheses)

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Armstrong Moore PNAS 2007

• Voluntary attention improves the discriminability
  of visual cortical responses to relevant stimuli
• Recent work implicates the frontal eye field in
  driving spatial attention
• Subthreshold microstimulation enhances V4 neural
  response, but it is unknown whether the
  enhancements include improved visual-response
  discriminability (part of voluntary attention)
• Armstrong and Moore explored response
  discriminability in this paper

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Solid as a ROC?

• Used receiver-operating characeristic (ROC)
  analysis to quantify how well v4 neurons could
  discriminate two stimuli
• Several hundred ms after visual stimulus onset,
  response adaptation had reduced the
  discriminability of V4 neurons to different
  stimuli
• Subthreshold microstimulation of FEF restored
  response discriminability

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Paradigm

• One of two differently oriented bars was
  presented in RF of single V4 neurons in monkey
• Monkey is performing a passive fixation task
• AROC is area under ROC curve, and is performance
  expected of an ideal observer making a decision
  about RF stimulus orientation based on neuron's
  response

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Visual Response Discriminability

• V4 response to 45º bar is higher than response to
  135º bar (figure 1a)
• AROC curve shows probability of perfect observer
  being able to discriminate stimuli based on V4
  response (figure 1b)
• Neurons with stimulus tuning during onset
  analysis window show higher discriminability
  (figure 1c)
• Discriminability decrease as a function of time
  (figure 1d)

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V4 Response Discriminability

• V4 response is enhanced with stimulation only
  when visual stimuls is oriented at 45º (figure
  2a)
• AROC is significantly higher for stimulation than
  for control (figure 2b)
• Discriminability is higher for stimulation
  neurons than control neurons (figure 2c)
• Effect of microstimulation on discrimination
  positively correlated with change in
  discriminability between onset and late trials
  (figure 2d)

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Visual Stimuli Spatial Alignment

• Subset of neurons tested with RF stimuli either
  spatially aligned or misaligned with saccade
  vector possibly evoked from stimulation site
• Microstimulation enhanced neuronal response
  discriminability for visual stimuli appearing at
  aligned RF position
• Microstimulation had no effect on neuronal
  response discriminability for visual stimuli
  appearing at the misaligned RF position

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Effect of Spatial Alignment

• When RF stimulus is aligned, stimulation enhances
  discriminability (figure 3a)
• When RF stimulus is misaligned, stimulation has
  no effect on discriminability (figure 3b)

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Response Reliability

• Regarding the relationship between response
  magnitude (spike count) and variance, power terms
  and coefficients were not significantly different
  for stimulation vs. control (figure 4a)
• Stimulation enhanced response to preferred
  stimuli, but not to non-preferred stimuli (figure
  4b)
• FEF microstimulation, like voluntary attention,
  improves response discriminaability without
  altering response reliability

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Timing and Simulated Phosphenes

• In the first poststimulation time bin (first 40
  ms), discriminability had already been
  significantly increased (figure 5a)
• Examined influence of simulated phosphene on
  response discriminability (figure 5b)
• Simulated phosphene disrupted response
  discriminability 70ms after phosphene onset
• Simulated phosphene is temporarily masking the
  stable RF stimulus when presented simultaneously

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The End

• Thanks

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The Human Brain
Precentral sulcus
Postcentral sulcus
Central sulcus