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Selecting information and selecting action Toward a unified account of attention

Selecting information and selecting action Toward a unified account of attention and decision making Jacqueline Gottlieb, PhD Department of Neuroscience Department of Psychiatry Columbia University. Why attention?. Attention is critical for cognition:

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Selecting information and selecting action Toward a unified account of attention

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  1. Selecting information and selecting action Toward a unified account of attention and decision making Jacqueline Gottlieb, PhD Department of Neuroscience Department of Psychiatry Columbia University

  2. Why attention? Attention is critical for cognition: it is the ability to concentrate on a task Failures of attention have devastating effects. Contralateral neglect: loss of awareness of space contralateral to a brain lesion. ADD/ADHD: inability to focus, severely disorganized behavior.

  3. Outline I. What is attention? A mechanism of information selection, which precedes decision formation. II. The lateral intraparietal area (LIP) is important for attention (information selection) a. Neurons encode cue selection b. Responses correlate with performance c. Neurons integrate top-down and bottom-up information d. Reversible inactivation affects performance III. Information selection is sensitive to decision variables a. Action selection b. Expected reward IV. Broader significance

  4. What IS attention? “Everyone knows what attention is.” William James, 1890 “…It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration is its essence […].” Attention is a form of selection. But what kind of selection? How is it related to decision-making? Difficult questions, not addressed by the research community.

  5. Neural mechanisms of decisions Neurons reflect the difficulty, timing, expected reward, and confidence of the decision. They provide a window on decision formation.

  6. These responses have been associated with action selection Sensory areas (e.g., MT) Cue Action 1 Action 2 Pre-motor areas (e.g., LIP)

  7. C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C C Additional evidence Other evidence suggests that LIP also responds to cues. But so far these responses are only bottom-up. Which C? In natural environments, cue selection is a difficult process. Does LIP also reflect top-down selection?

  8. Clarifying the distinction Attention: The decision: Operates on “action space” (buy, sell, wait). Operates on a huge stimulus space. Has flexible timing relative to the decision.

  9. I. What is attention? A mechanism of information selection, which precedes decision formation. II. The lateral intraparietal area (LIP) is important for attention (information selection) a. Neurons encode cue selection b. Responses correlate with performance c. Neurons integrate top-down and bottom-up information d. Reversible inactivation affects performance

  10. The task Right bar Left bar The cues: Attentional selection is demanding: the monkey has to FIND the instruction cue. Oristaglio et al. 2006, Balan and Gottlieb, 2009

  11. Search performance depends on the number of distractors Set size 2 Set size 4 Set size 6

  12. I. Activity encodes target location and depends on set-size 2 4 6 Balan and Gottlieb, 2008

  13. II. Target selectivity correlates with performance Correct 4 6 Errors Correlates with reaction times Absent on error trials Distractor response Target response Balan and Gottlieb, 2008

  14. Difference starts before PB III. Neurons integrate responses to bottom-up salience Abrupt change Search RELEVANT PB IRRELEVANT PB Balan and Gottlieb, 2006

  15. E E Balan and Gottlieb, 2009 IV. Reversible inactivation impairs target selection

  16. Outline I. What is attention? A mechanism of information selection, which precedes decision formation. II. The lateral intraparietal area (LIP) is important for top-down attention a. Neurons encode cue selection b. Responses correlate with performance c. Neurons integrate top-down and bottom-up information d. Reversible inactivation affects performance III. Information selection in LIP is coordinated with decision formation a. Action selection

  17. The task Right bar Left bar Decision not intended to activate neurons.

  18. And yet it does! Distractor in receptive field Target in receptive field Substantial, found in 40-70% of cells. Not due to target shape. Represents the right or left limb regardless of its location. Modulatory, not primary response. Oristaglio et al, 2006

  19. E E Is LIP a limb area? No. Inactivation does not affect manual release.

  20. Outline I. What is attention? Attention is a mechanism of information selection, which precedes decision formation. II. The lateral intraparietal area (LIP) is important for top-down attention Evidence from neural recording and inactivation III. Information selection in LIP is sensitive to decision formation a. Action selection b. Expected reward

  21. How should reward affect information? Conflicting requirements But we also have to process “bad news”. It may be desirable to attend to “good news” (e.g., get that ripe banana)

  22. Task Random location Outcome Reward delay (250 ms) Saccade to target Delay 600 ms Reward cue (RC) Fixation RF on a stimulus RC+: Reward RC- : No reward RC do not predict saccade direction. Peck et al, 2009

  23. However, LIP encodes RC valence RC+ RC- in RF Saccade target opposite RC+ RC- opposite in RF Peck et al, 2009

  24. The effect is spatially specific! Good news attract attention Bad news repel attention

  25. We can see it in the eye movements RC+ RC- RC+ RC- Away To Away To Maladaptive but persistent Strong and automatic effect of reward. Peck et al, 2009

  26. Outline I. What is attention? Attention is a mechanism of information selection, which precedes decision formation. II. The lateral intraparietal area (LIP) is important for top-down attention Evidence from neural recording and inactivation III. Information selection in LIP is sensitive to decision formation a. Action selection b. Expected reward IV. Broader significance

  27. Attention can be modeled as a form of decision Cues (Information) Consequences Actions C5 a1 C3 + C4 C2 a2 - C1 Select information (a “perceptual decision”) that is relevant to an action (“a manipulative decision”) that increases reward The value of information is “backed up” from the value of an action.

  28. Conclusions Neurons in LIP reflect the selection of information. These responses are sensitive to variables that affect decision formation (action, reward). Attention may be modeled as a sequential decision process: deciding which information is associated with an action that can harvest a reward.

  29. Thinking ahead 1. Implications for computational models of attention 2. Attentional priority may be related to the validity of a cue. 3. Attention may be modeled as a sequential decision. Learning the value of a cue requires a two-step value backup (to the action and then to the information). This may explain why stopping to attend is more difficult than acting impulsively.

  30. 1. The attentional feedback is differentiated along several dimensions (e.g., space AND orientation) Decision Sensory Reynolds & Heeger, Neuron 61(2): 168-185, 2009 LH (LE) This may make the feedback more efficient. Action RH (RE)

  31. 2. Are cues of different validity afforded different degrees of attention? Cues (Information) Consequences Actions C5 C3 a1 + C4 C2 a2 - C1 We want to attend to a cue that constrains our decision. A cue that does not constrain the decision is of little value.

  32. 3. Attention may be modeled as a sequential decision (TD learning?) Cues (Information) Consequences Actions C5 a1 C3 + C4 C2 a2 - C1 Select information (a “perceptual decision”) Then select an action (a “manipulative decision”) Then monitor the consequence The value of information is “backed up” from the value of an action.

  33. Sequential decision task: does LIP show backward learning? Preliminary data

  34. Transition contingencies Critical choice Non-critical choice Critical choice Non-critical choice Conflict: Choose A (or C) to get the large final reward, although B (or D) has the higher immediate reward. Choosing according to final reward is optimal.

  35. Performance Learning continues to improve; we artificially truncated the graph at 100 trials

  36. Example neuron One-back, critical stage (Stage -1) Optimal choices Preferred direction Null direction

  37. Neurons show some backward learning Specific for critical choice? Diminishes with distance from reward? Stage -1 Stage -2 One-back After learning Before learning Pref Null Pref Null Direction Target selection (Pref – Null) Learning effect (sp/s/trial) Two-back Pref Null Pref Null Direction Time before saccade Time before saccade Time after T on Time after T on

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