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Prefrontal cortex: categories, concepts and cognitive control Earl K. Miller

Prefrontal cortex: categories, concepts and cognitive control Earl K. Miller Picower Center for Learning and Memory, RIKEN-MIT Neuroscience Research Center, and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology www.millerlab.org. Sensory. Motor.

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Prefrontal cortex: categories, concepts and cognitive control Earl K. Miller

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  1. Prefrontal cortex: categories, concepts and cognitive control Earl K. Miller Picower Center for Learning and Memory, RIKEN-MIT Neuroscience Research Center, and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology www.millerlab.org

  2. Sensory Motor Executive (cognitive) control – The ability of the brain to wrest control of its processing from reflexive reactions to the environment in order to direct it toward unseen goals. Volition. Basic sensory and motor functions

  3. Sensory Motor Consolidation(long-term storage) Learning and memory Memories, habits and skills (Hippocampus, basal ganglia, etc.)

  4. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Sensory Motor Consolidation(long-term storage)

  5. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  6. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  7. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  8. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  9. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  10. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  11. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  12. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  13. Our Methods: Train monkeys on tasks designed to isolate cognitive operations related to executive control. Record from groups of single neurons while monkeys perform those tasks.

  14. Learning and memory (Hippocampus, basal ganglia, etc.) Executive Functionsgoal-related information Top-down Selection(flexibility) Sensory Motor Bottom-up Consolidation(long-term storage)

  15. Perceptual Categories David Freedman Maximillian RiesenhuberTomaso Poggio Earl Miller www.millerlab.org

  16. Perceptual Categorization: “Cats” Versus “Dogs” 60% Dog Morphs 60% Cat Morphs 80% Cat Morphs 80% Dog Morphs Prototypes 100% Dog Prototypes 100% Cat Category boundary Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2001) Science, 291:312-316 Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2002) J. Neurophysiology, 88:914-928.

  17. “Cats” Category boundary “Dogs”

  18. Perceptual Categorization: “Cats” Versus “Dogs” 60% Dog Morphs 60% Cat Morphs 80% Cat Morphs 80% Dog Morphs Prototypes 100% Dog Prototypes 100% Cat Category boundary Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2001) Science, 291:312-316 Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2002) J. Neurophysiology, 88:914-928.

  19. Delayed match to category task RELEASE(Category Match) . . . . (Match) Fixation Sample 500 ms. . HOLD (Category Non-match) Delay 600 ms. 1000 ms. Test Test object is a “match” if it the same category (cat or dog) as the sample (Nonmatch)

  20. Fixation Sample Delay Test 13 100% Dog P > 0.1 80:20 Dog:Cat 60:40 Dog:Cat 10 Firing Rate (Hz) Cats vs. DogsP < 0.01 7 4 100% Cat 80:20 Cat:Dog P > 0.1 60:40 Cat:Dog 1 -500 0 500 1000 1500 2000 Time from sample stimulus onset (ms) A “Dog Neuron” in the Prefrontal Cortex

  21. Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2001) Science, 291:312-316 Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K. (2002) J. Neurophysiology, 88:914-928 ??? Freedman, D.J., Riesenhuber, M., Poggio, T. and Miller, E.K, in prep.

  22. An ITC neuron that responded more strongly to DOGS than CATS.

  23. Delay Sample Time course of category-related activity:Inferior Temporal Cortex

  24. Delay Sample Time course of category-related activity:Prefrontal Cortex

  25. D1 C1 C1 D1 C1 C1 D2 D2 D3 C1 D3 C1 C2 D1 D1 D1 C2 C1 D2 C2 D2 D2 C2 C1 D3 D3 D3 C2 C2 C1 D1 D1 C3 C3 D1 C2 D2 C3 D2 C3 D2 C2 D3 D3 C3 D3 C3 C2 D1 C3 D2 C3 C2 D3 C3 ITC C3 C1 D1 C1 D2 C1 “cats” D3 C1 D1 C2 D2 C2 D3 C2 category boundary D1 C3 D2 C3 D3 C3 “dogs” D1 D3 D2 1.0 0.5 0 Normalized firing rate Category Effects were Stronger in the PFC than ITC: Single neurons Activity to individual stimuli along the 9 morph lines that crossed the category boundary PFC Cats Dogs Cats Dogs

  26. PFC ITC Category index values Stronger category effects Category Effects were Stronger in the PFC than ITC: Population Index of the difference in activity to stimuli from different, relative to same, category

  27. Quantity (numerosity) Andreas NiederDavid FreedmanEarl Miller www.millerlab.org

  28. Behavioral protocol: delayed-match-to-number task Release Numbers 1 – 5were used Hold • Preventing the monkey from memorizing visual patterns: • Position and size of dots shuffled pseudo-randomly. • Each numerosity tested with 100 different images per session. • All images newly generated after a session. • Sample and test images never identical. A. Nieder, D.J. Freedman, and E.K. Miller (2002) Science, 297:1708-1711.

  29. Trained Equal area Equal circumference Low density High density Variable features ‘Shape’ Linear Standard stimulus Monkeys instantly generalized acrossthe control stimulus sets.

  30. Standard stimulus Sample Delay Equal area Average sample interval activity

  31. Standard stimulus Sample Delay Variable features Average delay interval activity

  32. Low density Sample Delay High density Average sample interval activity

  33. Number-encoding neurons A. Nieder and E.K. Miller (in preparation) A. Nieder, D.J. Freedman, and E.K. Miller (2002)Science, 297:1708-1711. A. Nieder and E.K. Miller (in preparation)

  34. Proportion of number-selective neurons Prefrontal Cortex 33% N = 352 7% Parietal Cortex N = 404(area 7a: 222; SPL/ IPS: 180) Posterior Parietal Cortex:Single Neuron (area 7a) Standard stimulus Equal area

  35. Standard stimulus Low density Equal circumference High density Inferior Temporal Cortex

  36. Abstract number-encoding neurons Parietal CortexN = 404 Lateral PrefrontalCortexN = 352 Inferior Temporal CortexN = 77

  37. Behavior-guiding rules Jonathan WallisWael Asaad Kathleen AndersonGregor RainerEarl Miller www.millerlab.org

  38. CONCRETE ABSTRACT Asaad, Rainer, & Miller (1998)(also see Fuster, Watanabe,Wise et al) Asaad, Rainer, & Miller (2000)task context What is a rule? Rules describe the logic of a goal-directed task. Wallis et al (2001)

  39. Sample Test Release Hold Match Rule(same) Wallis, J.D., Anderson, K.C., and Miller, E.K. (2001) Nature, 411:953-956

  40. Sample Release Hold Sample Test Hold Release Nonmatch Rule(different) Test Wallis, J.D., Anderson, K.C., and Miller, E.K. (2001) Nature, 411:953-956

  41. Sample Release Hold Match Rule(same) Sample Test Hold Release Nonmatch Rule(different) Test The rules were made abstract by training monkeys until they couldperform the task with novel stimuli

  42. + juice OR Match + low tone + no juice OR Nonmatch + high tone Sample + Cue

  43. Match Neuron Cue

  44. Abstract rules Premotor cortex:Wallis, J.D. and Miller, E.K.(submitted) Wallis, J.D., Anderson, K.C., and Miller, E.K. (2001) Nature, 411:953-956

  45. Abstract Rule Coding in the Premotor Cortex (area 6)

  46. TEST SAMPLE TEST PFC SAMPLE PFC PMC PMC ROC Value Proportion of values ROC Value Time from sample onset (ms) Number of neurons(All recorded neurons) Abstract Rule-Encoding in the PFC vs. PMC

  47. CONCLUSIONS: 1. Goal-related information, including the categories and concepts needed for executive control, is represented in the PFC while irrelevant details are largely discarded. 2. Neural representations of categories and concepts are stronger and more explicit in the PFC than in cortical areas that provide the PFC with visual input(“cats and dogs”, numbers). But well-learned rules are more strongly encoded in PMCthan PFC. 3. This ability of the PFC and related areas to convey categories, concepts and rules may reflect their role in acquiring and representing the formal demands of tasks, the internal models of situations and courses of actionthat provide a foundation for complex, intelligent behavior. A Model of PFC function:Miller, E.K. (2000) The prefrontal cortex and cognitive control. Nature Reviews Neuroscience, 1:59-65 Miller, E.K. and Cohen, J.D. (2001) An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24:167-202 For reprints etc: www.millerlab.org

  48. The PF cortex and cognitive control Phone rings Answer Don’t answer Inactive Active

  49. The PF cortex and cognitive control At home Guest Phone rings Answer Don’t answer Inactive Active

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