Are We Paying Attention Yet?

1. Are We Paying Attention Yet? A review of the relation between attention and saccades By Travis McKinney

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

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?

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

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.

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

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

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

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

10. Comparison between studies • Exogenous cueing: Yellow Foci • Endogenous cueing: Red Foci • Parietal and Frontal regions coactivate when locations are cued exogenously and endogenously

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

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

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

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

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

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

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

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

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

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 monkey’s ability to covertly filter visual stimuli

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)

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)

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)

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

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

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 • 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

27. 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)

28. 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)

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

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)

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

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

33. The End • Thanks

34. The Human Brain Precentral sulcus Postcentral sulcus Central sulcus