Autonomous encoding of irrelevant goals and outcomes by prefrontal cortex neurons

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1970-1978

  Genovesio, Aldo ^a   Tsujimoto, Satoshi ^b   Navarra, Giulia ^a   Falcone, Rossella ^a   Wise, Steven P ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Nielsen NeuroFocus   (Japan)

^c Olschefskie Institute for the Neurobiology of Knowledge   (United States)

Author keywords

Memory; Monitoring; Monkey; Prefrontal; Spatial

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISCRIMINATION LEARNING; EYE POSITION; HISTOLOGY; MALE; NEUROPHYSIOLOGICAL MONITORING; NONHUMAN; PERCEPTIVE DISCRIMINATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; TASK PERFORMANCE; VISUAL DISCRIMINATION; VISUAL STIMULATION;

MEMORY; MONITORING; MONKEY; PREFRONTAL; SPATIAL;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CHOICE BEHAVIOR; COLOR PERCEPTION; DISTANCE PERCEPTION; ELECTROLYSIS; GOALS; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; REACTION TIME; ROC CURVE; TIME FACTORS;

EID: 84893046611     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3228-13.2014     Document Type: Article

References (53)

1. Barraclough DJ, Conroy ML, Lee D (2004) Prefrontal cortex and decision making in a mixed-strategy game. Nat Neurosci 7: 404-410. CrossRef Medline
2. Bernacchia A, Seo H, Lee D, Wang XJ (2011) A reservoir of time constants for memory traces in cortical neurons. Nat Neurosci 14: 366-372. CrossRef Medline
3. Bichot NP, Schall JD (1999) Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci 2: 549-554. CrossRef Medline
4. Cai X, Kim S, Lee D (2011) Heterogeneous coding of temporally discounted values in the dorsal and ventral striatum during intertemporal choice. Neuron 69: 170-182. CrossRef Medline
5. Chen NH, White IM, Wise SP (2001) Neuronal activity in dorsomedial frontal cortex and prefrontal cortex reflecting irrelevant stimulus dimensions. Exp Brain Res 139: 116-119. CrossRef Medline
6. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18: 193-222. CrossRef Medline
7. Duncan J (2010) The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 14: 172-179. CrossRef Medline
8. Everling S, Tinsley CJ, Gaffan D, Duncan J (2006) Selective representation of task-relevant objects and locations in the monkey prefrontal cortex. Eur J Neurosci 23: 2197-2214. CrossRef Medline
9. Funahashi S, Bruce CJ, Goldman-Rakic PS (1993) Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas. " J Neurosci 13: 1479-1497. Medline
10. Genovesio A, Brasted PJ, Mitz AR, Wise SP (2005) Prefrontal cortex activity related to abstract response strategies. Neuron 47: 307-320. CrossRef Medline
11. Genovesio A, Brasted PJ, Wise SP (2006a) Representation of future and previous spatial goals by separate neural populations in prefrontal cortex. J Neurosci 26: 7305-7316. CrossRef Medline
12. Genovesio A, Tsujimoto S, Wise SP (2006b) Neuronal activity related to elapsed time in prefrontal cortex. J Neurophysiol 95: 3281-3285. CrossRef Medline
13. Genovesio A, Tsujimoto S, Wise SP (2008) Encoding problem-solving strategies in prefrontal cortex: activity during strategic errors. Eur J Neurosci 27: 984-990. CrossRef Medline
14. Genovesio A, Tsujimoto S, Wise SP (2009) Feature-and order-based timing representations in the frontal cortex. Neuron 63: 254-266. CrossRef Medline
15. Genovesio A, Tsujimoto S, Wise SP (2011) Prefrontal cortex activity during the discrimination of relative distance. J Neurosci 31: 3968-3980. CrossRef Medline
16. Genovesio A, Tsujimoto S, Wise SP (2012) Encoding goals but not abstract magnitude in the primate prefrontal cortex. Neuron 74: 656-662. CrossRef Medline
17. Histed MH, Pasupathy A, Miller EK (2009) Learning substrates in the primate prefrontal cortex and striatum: sustained activity related to successful actions. Neuron 63: 244-253. CrossRef Medline
18. Ito S, Stuphorn V, Brown JW, Schall JD (2003) Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302: 120-122. CrossRef Medline
19. Kennerley SW, Wallis JD (2009) Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables. Eur J Neurosci 29: 2061-2073. CrossRef Medline
20. Kennerley SW, Walton ME (2011) Decision making and reward in frontal cortex: complementary evidence from neurophysiological and neuropsychological studies. Behav Neurosci 125: 297-317. CrossRef Medline
21. Kennerley SW, Behrens TE, Wallis JD (2011) Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat Neurosci 14: 1581-1589. CrossRef Medline
22. Kim S, Hwang J, Lee D (2008) Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59: 161-172. CrossRef Medline
23. Lauwereyns J, Sakagami M, Tsutsui K, Kobayashi S, Koizumi M, Hikosaka O (2001) Responses to task-irrelevant visual features by primate prefrontal neurons. J Neurophysiol 86: 2001-2010. Medline
24. Mann SE, Thau R, Schiller PH (1988) Conditional task-related responses in monkey dorsomedial frontal cortex. Exp Brain Res 69: 460-468. Medline
25. Mansouri FA, Matsumoto K, Tanaka K (2006) Prefrontal cell activities related to monkeys' success and failure in adapting to rule changes in a Wisconsin Card Sorting Test analog. J Neurosci 26: 2745-2756. CrossRef Medline
26. Owen AM, Evans AC, Petrides M (1996) Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cereb Cortex 6: 31-38. CrossRef Medline
27. Passingham RE, Wise SP (2012) The neurobiology of the prefrontal cortex: anatomy, evolution, and the origin of insight. Oxford: Oxford UP.
28. Petrides M (2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360: 781-795. CrossRef Medline
29. Rainer G, Asaad WF, Miller EK (1998) Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393: 577-579. CrossRef Medline
30. Rainer G, Rao SC, Miller EK (1999) Prospective coding for objects in primate prefrontal cortex. J Neurosci 19: 5493-5505. Medline
31. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81: 1903-1916. Medline
32. Rigotti M, Barak O, Warden MR, Wang XJ, Daw ND, Miller EK, Fusi S (2013) The importance of mixed selectivity in complex cognitive tasks. Nature 497: 585-590. CrossRef Medline
33. Roesch MR, Olson CR (2003) Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex. J Neurophysiol 90: 1766-1789. CrossRef Medline
34. Saito N, Mushiake H, Sakamoto K, Itoyama Y, Tanji J (2005) Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period. Cereb Cortex 15: 1535-1546. CrossRef Medline
35. Samejima K, Ueda Y, Doya K, Kimura M (2005) Representation of actionspecific reward values in the striatum. Science 310: 1337-1340. CrossRef Medline
36. Schoenbaum G, Eichenbaum H (1995) Information coding in the rodent prefrontal cortex. 1. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J Neurophysiol 74: 733-750. Medline
37. Schultz W (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30: 259-288. CrossRef Medline
38. Seo H, Lee D (2007) Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. J Neurosci 27: 8366-8377. CrossRef Medline
39. Seo H, Barraclough DJ, Lee D (2007) Dynamic signals related to choices and outcomes in the dorsolateral prefrontal cortex. Cereb Cortex 17: i110-i117. CrossRef Medline
40. Seo H, Barraclough DJ, Lee D (2009) Lateral intraparietal cortex and reinforcement learning during a mixed-strategy game. J Neurosci 29: 7278-7289. CrossRef Medline
41. Sigala N, Kusunoki M, Nimmo-Smith I, Gaffan D, Duncan J (2008) Hierarchical coding for sequential task events in the monkey prefrontal cortex. Proc Natl Acad Sci U S A 105: 11969-11974. CrossRef Medline
42. Simmons JM, Richmond BJ (2008) Dynamic changes in representations of preceding and upcoming reward in monkey orbitofrontal cortex. Cereb Cortex 18: 93-103. CrossRef Medline
43. Takeda K, Funahashi S (2007) Relationship between prefrontal task-related activity and information flow during spatial working memory performance. Cortex 43: 38-52. CrossRef Medline
44. Tanji J, Hoshi E (2008) Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88: 37-57. CrossRef Medline
45. Tsujimoto S, Postle BR (2012) The prefrontal cortex and oculomotor delayed response: a reconsideration of the "mnemonic scotoma. " J Cogn Neurosci 24: 627-635. CrossRef Medline
46. Tsujimoto S, Sawaguchi T (2004) Neuronal representation of responseoutcome in the primate prefrontal cortex. Cereb Cortex 14: 47-55. CrossRef Medline
47. Tsujimoto S, Sawaguchi T (2005) Context-dependent representation of response-outcome in monkey prefrontal neurons. Cereb Cortex 15: 888-898. CrossRef Medline
48. Tsujimoto S, Genovesio A, Wise SP (2008) Transient neuronal correlations underlying goal selection and maintenance in prefrontal cortex. Cereb Cortex 18: 2748-2761. CrossRef Medline
49. Tsujimoto S, Genovesio A, Wise SP (2012) Neuronal activity during a cued strategy task: comparison of dorsolateral, orbital, and polar prefrontal cortex. J Neurosci 32: 11017-11031. CrossRef Medline
50. Wallis JD, Miller EK (2003) Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18: 2069-2081. CrossRef Medline
51. Wallis JD, Anderson KC, Miller EK (2001) Single neurons in prefrontal cortex encode abstract rules. Nature 411: 953-956. CrossRef Medline
52. Wirth S, Avsar E, Chiu CC, Sharma V, Smith AC, Brown E, Suzuki WA (2009) Trial outcome and associative learning signals in the monkey hippocampus. Neuron 61: 930-940. CrossRef Medline
53. Yamagata T, Nakayama Y, Tanji J, Hoshi E (2012) Distinct information representation and processing for goal-directed behavior in the dorsolateral and ventrolateral prefrontal cortex and the dorsal premotor cortex. J Neurosci 32: 12934-12949. CrossRef Medline