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The vanishing central executiveDistributed neural mechanisms of decision-making                     Paul Cisek        Summ...
Our question:• When, where, how and why — since the origin of life on Earth  about 4 billion years ago — did organisms inp...
What is behavior?sensory                                                                     motor             Perception ...
Psychological architecture for behaviorsensory                                                                     motor  ...
“Dualism”sensory                                                                 motor                Perception          ...
Behaviorismsensory                                                 motor               Perception          Mind        Act...
Behaviorismsensory                                                                   motor                Perception      ...
Cognitivismsensory                                               motor             Perception                      Action ...
Cognitivismsensory                                                                 motor               Perception         ...
Computational view of the brain•   The “computer metaphor”    – Cognition is like computation:      Rule-based manipulatio...
What kinds of representations?•   “Descriptive” representations     –   Capture knowledge about the world         and the ...
Can we use this to understand the brain?•   Cognitive Neuroscience     – How are psychological /       cognitive functions...
Where is the central representation?•   The visual system    – Two visual processing streams:        •   ventral “what”   ...
Perception, Cognition, & Action Systems?•   Primary sensory and motor regions•   “Association” regions    – Appear to firs...
Where is the central executive?•   Decision-making    – Neural correlates in prefrontal      and orbitofrontal cortex    –...
Conceptual challenges• The binding problem   – How to create the unified representation of the world that is needed     as...
Psychological architecture for behaviorsensory                                                               motor        ...
Evolution         •   Two key concepts:             – Natural selection                 • What is the selective advantage ...
The long history of behavior
Are brains input/output devices?• What else could they be?
What kinds of devices are living systems?• Control systems:   – Ex: Biochemistry       • Suppose there is some substance A...
What kinds of devices are living systems?• Control systems can extend beyond the skin   – Ex: Kinesis                     ...
Different ways of looking at behavior1. Given a perception, produce the best action   “The whole neural organism, it will ...
Ethology•   Studies of animal behavior in                      Von Uexküll    the wild•   Species-specific behavioral    n...
What kinds of representations?•   “Descriptive” representations                  •   “Pragmatic” representations     –   C...
Example: Decision-makingWhat to do? Move the queen? Protect the pawn? Threaten the  knight?                               ...
Decision-making in the wild•   The world presents animals with multiple opportunities for action (“affordances”)•   Cannot...
Action specification and selectionmust occur in parallel
Sensorimotor contingencies influencehow selection should be done
Specification and selection in parallel                                               A population of tuned neurons       ...
What are the neural substrates?
attention   Specification in the dorsal visual stream             –   Cells sensitive to spatial visual information       ...
potential actionsattention                       Fronto-parietal system                         –      Activity related to...
potential actionsattention                 behavioral                 biasing                       Basal ganglia         ...
potential actionsattention                                          cognitive                                         deci...
potential actionsattention                                                                  cognitive                     ...
potential actionsattention                                                                  cognitive                     ...
“Affordance competition hypothesis”                                       potential actions   Cisek (2007) Phil.Trans.Roya...
Behavior          Perception                                     Cognition                                    Action      ...
Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Eve...
Neural activity specifies multiple actions                                      Classic model:                            ...
Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Eve...
Biased choice task1-TARGET                                       1 drop       Alexandre   CHT                             ...
Neural activity in premotor cortex•   No effect of value    in 1T task•   However, if another    target is present, then  ...
Distance-dependent interactions                •   More activity when targets are                    closer               ...
Why should it matter that distance matters?• The distance effect suggests that the decision is made  within the sensorimot...
Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Eve...
potential actionsattention                                                                  cognitive                     ...
Timing                                       potential actions• An animal is constantly interacting with the worldattentio...
potential actionsattention                                                                  cognitive                     ...
potential actionsWave 1. Fast feedforward sweep
potential actionsattention                                               cognitive                                        ...
Two waves of activityLedberg et al. (2007) Cerebral Cortex •   Measured LFPs from various regions of cerebral cortex •   M...
Two waves of activity1. Fast feedforward sweep    •   Activation in ~50ms        throughout dorsal        stream and front...
Summary 1: Experimental data• Simultaneous specification of multiple potential actions    – Arm reaching system (PMd, PRR,...
Summary 2: Theoretical concepts•   “Affordance competition hypothesis”     – Instead of serial Perception, Cognition, & Ac...
Summary 3: Philosophical implications•   There is no central executive     – Decisions emerge through a distributed consen...
“The great end of life is not knowledge but action”                  – T. H. Huxley                    (1825-1895)“Your he...
THANK YOU•   Lab members    –   Marie-Claude Labonté    –   Alexandre Pastor-Bernier    –   David Thura    –   Ignasi Cos ...
Paul Cisek Model - No "Decision" "Decision-Making"
Paul Cisek Model - No "Decision" "Decision-Making"
Paul Cisek Model - No "Decision" "Decision-Making"
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Paul Cisek Model - No "Decision" "Decision-Making"

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The vanishing central executive - Distributed neural mechanisms of decision-making

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  • Brilliant work and great alternative to the dominant, popular culture notions of "cognitive" neuroscience.
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Paul Cisek Model - No "Decision" "Decision-Making"

  1. 1. The vanishing central executiveDistributed neural mechanisms of decision-making Paul Cisek Summer School in Cognitive Sciences Evolution and Function of Consciousness July 4, 2012
  2. 2. Our question:• When, where, how and why — since the origin of life on Earth about 4 billion years ago — did organisms input/output functions become conscious input/output functions? But first, another question:• Why “input/output” functions?
  3. 3. What is behavior?sensory motor Perception Cognition Action input output representation representation of the world of the motor plan “The whole neural organism, it will be remembered, is, physiologically considered, but a machine for converting stimuli into reactions” (James, 1890, p. 372). Behavior: An analysis of the world, followed by deliberation and planning, followed by execution of the plan. William James “sense, think, act”
  4. 4. Psychological architecture for behaviorsensory motor Perception Cognition Action input output representation representation of the world of the motor plan • University courses • Textbooks Q: From where does this view originate? • Journals • Conferences • Academic departments • Grant review committees • Scientists • Questions we ask • Theories we propose
  5. 5. “Dualism”sensory motor Perception Mind Action input output Socrates Descartes • Philosophy: The mind is non-physical – This forces interfaces between non- physical mind and physical world • Psychology: Study of the psyche – Structuralism: The mind is studied through introspection John Locke Wilhelm Wundt
  6. 6. Behaviorismsensory motor Perception Mind Action input output – Stop this metaphysical nonsense… John Watson
  7. 7. Behaviorismsensory motor Perception Action input output – Stop this metaphysical nonsense… – Perception and Action are directly linked – Subject matter: Learning laws which establish the linkage John Watson Ivan Pavlov Edward Thorndike B.F. Skinner
  8. 8. Cognitivismsensory motor Perception Action input output – Internal processes are indispensable Tolman
  9. 9. Cognitivismsensory motor Perception Cognition Action input output – Internal processes are indispensable Tolman Shannon – Cognition takes the mind’s place – A fully physical process – but what kind? – “Information processing” • Definition of “information” • Definition of “processing” – Cognition is a computational process Turing • Linguistics Chomsky • Language of thought Fodor
  10. 10. Computational view of the brain• The “computer metaphor” – Cognition is like computation: Rule-based manipulation of representations (Newell & Simon, Pylyshyn) – The mind is the software (Block) Newell & Simon – Studies of mental phenomena may be conducted independently of studies of brain physiology • Less to worry about • Not so much known (yet) about the brain • Historical separation between psychology and biology
  11. 11. What kinds of representations?• “Descriptive” representations – Capture knowledge about the world and the organism – Explicit – Objective, accurate to external Descriptive representations reality, uncontaminated by internal delineate the conceptual borders states input/output – Examples: between the processes that • ^ Reconstructed visual image • construct them and the 3-D map of the world input/output • Labeled objects processes that use them. • Desired path of the hand in space ^ David Marr
  12. 12. Can we use this to understand the brain?• Cognitive Neuroscience – How are psychological / cognitive functions produced by the brain? – Ex: Decision-making – Based on the concepts of cognitivism • Computation, descriptive representations, working memory, attentional filters, Michael Gazzaniga motor programs, etc.
  13. 13. Where is the central representation?• The visual system – Two visual processing streams: • ventral “what” • where dorsal “where” – Separate regions analyze color, motion, form, etc. – Separate regions for near and far space what• Binding problem – How to create the unified representation of the world that is needed as input for cognition?
  14. 14. Perception, Cognition, & Action Systems?• Primary sensory and motor regions• “Association” regions – Appear to first encode sensory, then motor representations Cognition? Cognition – Even true at the level of Cognition individual neurons Example: Lateral intraparietal area – is it “attention”? (input to cognition) – or “intention”? (output of cognition) – How could it be both? – Could it be cognition?
  15. 15. Where is the central executive?• Decision-making – Neural correlates in prefrontal and orbitofrontal cortex – also in parietal cortex – Premotor cortex – Supplemental motor area – Frontal eye fields – Basal ganglia – Even the superior colliculus – Activity reflects decision everywhere at about the same time (~150ms)
  16. 16. Conceptual challenges• The binding problem – How to create the unified representation of the world that is needed as input for cognition?• The problem of meaning – How does a computational process know the meaning of the representations that it manipulates? – “Chinese Room” (Searle) – The “symbol grounding problem” (Harnad) – Representations are purely syntactic, they have no intrinsic input/output semantics, no meaning to the system that uses them ^
  17. 17. Psychological architecture for behaviorsensory motor Perception Cognition Action input output • Some observations: 1. This model inherits its structure from mind-body dualism 2. Was designed to explain the abstract problem-solving behavior of adult humans 3. Its concepts were developed under the explicit assumption that the substrate doesn’t matter • Perhaps it should not be surprising that this model has difficulty explaining neural data…
  18. 18. Evolution • Two key concepts: – Natural selection • What is the selective advantage of X?Darwin – Descent with modification • What are the phylogenetic origins of X?
  19. 19. The long history of behavior
  20. 20. Are brains input/output devices?• What else could they be?
  21. 21. What kinds of devices are living systems?• Control systems: – Ex: Biochemistry • Suppose there is some substance A necessary A for survival • Suppose there’s a catalyst for creating A whose action is regulated inversely by the concentration of A • Feedback control system • Exploits consistencies in the laws of chemistry • Control loop within the organism: “Physiology”
  22. 22. What kinds of devices are living systems?• Control systems can extend beyond the skin – Ex: Kinesis B • Suppose substance B cannot be produced A within the body, must be absorbed from the world • If the local concentration of substance B falls below desired levels, move randomly • Exploits statistics of nutrient distributions (assumes that there is more elsewhere) Concentration of [B] • Control loop that extends outside the skin: “Behavior” – Reliable motor-sensory contingencies exist • Statistics of food distributions (move → find food) • Laws of optics and mechanics (contract muscle → arm moves) • Laws of interaction (you show teeth → I back off)• Animals are constantly doing whatever brings them to the most desirable situation (full stomach, safety, etc.) • “Behavior: The control of perception” (Powers, 1973)
  23. 23. Different ways of looking at behavior1. Given a perception, produce the best action “The whole neural organism, it will be remembered, is, physiologically considered, but a machine for converting stimuli into reactions” (James, 1890). William James2. Of the possible actions, produce that which results in the best perception “What we have is a circuit… the motor response determines the stimulus, just as truly as sensory stimulus determines movement” (Dewey, 1896). John Dewey
  24. 24. Ethology• Studies of animal behavior in Von Uexküll the wild• Species-specific behavioral niches• “Closed-loop” sensorimotor control• Key stimuli Lorenz & Von Holst Tinbergen
  25. 25. What kinds of representations?• “Descriptive” representations • “Pragmatic” representations – Capture knowledge about the world – Used to guide interaction between and the organism the world and the organism – Explicit – Implicit – Objective, accurate to external – Subjective, mix external reality and reality, uncontaminated by internal internal state, often correlate with many variables at once states – Examples: – Examples: • Salience map • Reconstructed visual image • Motor signals to the limb • 3-D map of the world • Subject-dependent opportunities for • Labeled objects action (“affordances”) • Desired path of the hand in space David Marr J.J. Gibson
  26. 26. Example: Decision-makingWhat to do? Move the queen? Protect the pawn? Threaten the knight? How to do it? Which grasp point?“Selection” What trajectory? How to avoid obstacles? “Specification” • Classical model: – First decide what to do (select) then plan the movement (specify) – Sense, think, act
  27. 27. Decision-making in the wild• The world presents animals with multiple opportunities for action (“affordances”)• Cannot perform all actions at the same time• Real-time activity is constantly modifying affordances, introducing new ones, etc.
  28. 28. Action specification and selectionmust occur in parallel
  29. 29. Sensorimotor contingencies influencehow selection should be done
  30. 30. Specification and selection in parallel A population of tuned neurons Distance Cell activity Direction• Action Specification: Activation of parameter regions corresponding to potential actions• Action Selection: Competition between distinct regions of activity
  31. 31. What are the neural substrates?
  32. 32. attention Specification in the dorsal visual stream – Cells sensitive to spatial visual information (Ungerleider & Mishkin …) – Involved in action guidance (Milner & Goodale) – Divergence into separate sub-streams, each specialized toward different kinds of actions (Stein; Andersen; Colby & Goldberg; Matelli & Luppino ...) – An increasing influence of attentional effects, enhancing information from particular regions of interest (Duncan & Desimone; Posner & Gilbert; Treue; Boynton ...) – Parietal representation of external world is “sparse” (Goldberg)
  33. 33. potential actionsattention Fronto-parietal system – Activity related to potential motor actions (Andersen; Georgopoulos; Kalaska; Wise; Hoshi & Tanji) – Competition between potential actions – Various biasing factors • attention (Goldberg; Steinmetz) • behavioral relevance (Mountcastle; Seal & Gross) • probability (Glimcher; Shadlen) • reward (Glimcher; Olson)
  34. 34. potential actionsattention behavioral biasing Basal ganglia – Cortico-striatal-pallido-thalamo-cortical loops (Alexander; Middleton & Strick) – Selection of actions from among alternatives (Mink; Redgrave et al.) – Reward (Hikosaka; Schultz)
  35. 35. potential actionsattention cognitive decision-making behavioral biasing Prefrontal cortex – High-level decisions based on knowledge object about object identity identity (Fuster; Miller; Tanji…) – Receives ventral stream information on object identity (Sakata…)
  36. 36. potential actionsattention cognitive decision-making predicted behavioral feedback biasing Execution – Fast visual feedback (Prablanc; Desmurget) object – Forward models identity (Ito; Wolpert; Miall) visual feedback motor command
  37. 37. potential actionsattention cognitive decision-making predicted behavioral feedback biasing object identity visual feedback motor command
  38. 38. “Affordance competition hypothesis” potential actions Cisek (2007) Phil.Trans.Royal Soc. B.•attention Continuous specification of currently available potential actions cognitive decision-making• Competition between potential action representations in fronto- parietal regions• Biasing from frontal and subcortical areas predicted behavioral feedback biasing• Decision is made through a “distributed consensus” object identity visual feedback motor command
  39. 39. Behavior Perception Cognition Action audition attention propositionalproprioception vision logic forward inverse decision planning models kinematics making object vision trajectory action recognition of space reinforcement generation sequencing learning Behavior Action Action specification selection decision grasping reaching running attention making affect reinforcement forward vision proprio- inverse arm key stimulus action learning kinematics detection arm models of nearby ception sequencing space object propositional recognition logic
  40. 40. Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Everything occurs in parallel
  41. 41. Neural activity specifies multiple actions Classic model: – Store information, decide, then plan one action Affordance competition: – Specify both actions, then select one Time Ce CePrimary llll P PD Motor DCortex Caudal PMd Rostral PMd Cisek & Kalaska (2005) Neuron
  42. 42. Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Everything occurs in parallel
  43. 43. Biased choice task1-TARGET 1 drop Alexandre CHT 2 drops Pastor-Bernier DELAY 3 drops GO THT Reward: 1 GO2-TARGET FREE THT CHT Reward: 3 DELAY 67% GO THT 33% FORCED Reward: 1
  44. 44. Neural activity in premotor cortex• No effect of value in 1T task• However, if another target is present, then activity increases with value of preferred target• If value of preferred target is constant, activity decreases with value of other target• Activity decreases with distance between targets Pastor-Bernier & Cisek (2011) J. Neurosci.
  45. 45. Distance-dependent interactions • More activity when targets are closer • Compare the strength of the competition as a function of target distance – As distance increases, slope is increasingly negative • The competition is strongest between cells with the largest difference in preferred directions
  46. 46. Why should it matter that distance matters?• The distance effect suggests that the decision is made within the sensorimotor system – If decisions were purely cognitive (“I prefer to get 3 drops of juice over 1 drop”), then they should be determined in an abstract space – The dynamics of the competition which determines choice depend on the spatial relationship between the movements themselves
  47. 47. Predictions• Multiple potential actions can be specified simultaneously• Biased competition between potential actions• Everything occurs in parallel
  48. 48. potential actionsattention cognitive decision-making predicted behavioral feedback biasing object identity visual feedback motor command
  49. 49. Timing potential actions• An animal is constantly interacting with the worldattention – Continuous sensorimotor control of ongoing actions cognitive decision-making – Continuous specification of alternative actions – Continuous evaluation of value – Continuous tradeoffs between persisting in a given activity or switching to a different, currently available one predicted behavioral feedback biasing• Specification and selection must normally occur in parallel• However, if we put the animal in the lab – Time is broken into discrete “trials”object of which begins with a each stimulus and ends with a responseidentity – The stimulus is deliberately made independent from the response• What should we see? motor visual feedback command
  50. 50. potential actionsattention cognitive decision-making predicted behavioral feedback biasing object identity visual feedback motor command
  51. 51. potential actionsWave 1. Fast feedforward sweep
  52. 52. potential actionsattention cognitive decision-making behavioral biasing object identity Wave 2. Attentional/Decisional modulation
  53. 53. Two waves of activityLedberg et al. (2007) Cerebral Cortex • Measured LFPs from various regions of cerebral cortex • Monkeys performed a conditional GO / NOGO task
  54. 54. Two waves of activity1. Fast feedforward sweep • Activation in ~50ms throughout dorsal stream and frontal cortex2. Attentional/Decisional • About 150ms post- stimulus, discrimination of Go/Nogo throughout the cortex
  55. 55. Summary 1: Experimental data• Simultaneous specification of multiple potential actions – Arm reaching system (PMd, PRR, M1) – Grasping system (AIP, PMv) – Saccade system (LIP, FEF, Superior colliculus)• Biased competition – Potential actions compete against each other within sensorimotor maps, influenced by a variety of biasing factors (e.g. reward) – NOTE: Similar mechanism as attention (Duncan & Desimone) • “Attention” is selection near sensors, “decision” is selection near effectors – Influences depend on geometry – decisions are not simply abstract • These are “pragmatic” representations, not “descriptive” – Decision is made through a “distributed consensus”• Parallel specification and selection systems
  56. 56. Summary 2: Theoretical concepts• “Affordance competition hypothesis” – Instead of serial Perception, Cognition, & Action modules, we have parallel specification and selection systems – Better match to neural data – Better suited to the kinds of tasks that dominated animal behavior• “Pragmatic representations” – Neural activity aimed not at describing the world, but at mediating interaction with the world – Correlation with external and internal variables is necessary, but mixtures are useful (e.g. spatial direction mixed with reward values) – Conjecture: Most, but not all, neural activity is of this kind • “Descriptive” representations (e.g. in the ventral stream) emerged in evolution as specializations of pragmatic representations for advanced selection• Cognitive advances evolved through hierarchical elaboration – Diversification of fronto-parietal loops, cortico-striatal circuits, cortico- cerebellar circuits, into progressively anterior/abstract systems – Interaction lays the foundation for cognition (Piaget)
  57. 57. Summary 3: Philosophical implications• There is no central executive – Decisions emerge through a distributed consensus• Classic problems in a different context – Binding problem: • Activity of separate streams is coherent by virtue of dealing with the same world – Symbol grounding problem: • Interaction has meaning by virtue of influencing the variables critical for life • Symbols are specializations (“shorthand notation”) that emerged late in evolution, already within the context of grounded interaction – The “Hard” problem • Feeling is different than doing – Being inside the loop is different than observing it from the outside – Private language, beetle in box, squirrel in head, 1 st person perspective, the “Umwelt”• The computer metaphor – With all due respect to Alan Turing, the computer metaphor is misleading as a model for the brain – What matters is control (Wiener, Ashby, Powers, Gibson, Dewey, etc.)
  58. 58. “The great end of life is not knowledge but action” – T. H. Huxley (1825-1895)“Your head is there to move you around” – R.E.M. (1980-2011)
  59. 59. THANK YOU• Lab members – Marie-Claude Labonté – Alexandre Pastor-Bernier – David Thura – Ignasi Cos – Matthew Carland – Jessica Trung• Alumni – Jean-Philippe Thivierge – Thomas Michelet – Valeriya Gritsenko EJLB THE FOUNDATION paul.cisek@gmail.com

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