Are We Paying Attention Yet? A review of the relation between
attention and saccades By Travis McKinney Slide 2 Overview
Corbetta: Covert vs. Overt Orienting -> fMRI and PET Moore and
Armstrong: FEF stimulation-> V4 response activity Moore and
Armstrong: FEF Stimulation -> V4 discriminability similar to
attention effects Slide 3 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? Slide 4 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 Slide
5 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. Slide 6 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 Slide 7 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 Slide 8 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 Slide 9 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 Slide 10 Comparison
between studies Exogenous cueing: Yellow Foci Endogenous cueing:
Red Foci Parietal and Frontal regions coactivate when locations are
cued exogenously and endogenously Slide 11 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
Slide 12 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 Slide 13 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
Slide 14 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
Slide 15 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 Slide 16 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
Slide 17 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 Slide 18 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 Slide 19 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 Slide 20 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 Slide 21 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) Slide 22 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)
Slide 23 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) Slide
24 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 Slide 25 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 Slide 26 Paradigm One of two
differently oriented bars was presented in RF of single V4 neurons
in monkey Monkey is performing a passive fixation task A ROC 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 Slide 27 Visual Response Discriminability V4
response to 45 bar is higher than response to 135 bar (figure 1a) A
ROC 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) Slide 28 V4 Response Discriminability
V4 response is enhanced with stimulation only when visual stimuls
is oriented at 45 (figure 2a) A ROC 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) Slide 29 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 Slide 30 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) Slide 31
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 Slide 32 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 Slide 33 The End Thanks Slide 34 Precentral sulcus
Central sulcus Postcentral sulcus The Human Brain
