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 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

27. Visual Response Discriminability V4 response to 45º bar is higher than response to 135º 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)

28. V4 Response Discriminability V4 response is enhanced with stimulation only when visual stimuls is oriented at 45º (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)

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. Precentral sulcus Central sulcus Postcentral sulcus The Human Brain