Apparent encoding of sequential context in rat medial prefrontal cortex is accounted for by behavioral variability

Journal of Neuroscience

Volumn 26, Issue 51, 2006, Pages 13143-13155

  Euston, David R ^a   McNaughton, Bruce L ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Delayed alternation; Prefrontal; Prelimbic cortex; Rat; Sequence disambiguation; Working memory

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CELL FUNCTION; CODING; CONTROLLED STUDY; MALE; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAILWAY; RAT; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY;

ACTION POTENTIALS; ANIMALS; MALE; MAZE LEARNING; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; RATS; RATS, INBRED BN; RATS, INBRED F344; REACTION TIME; REWARD;

EID: 33845792437     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3803-06.2006     Document Type: Article

References (54)

1. Aggleton JP, Neave N, Nagle S, Sahgal A (1995) A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions. J Neurosci 15:7270-7281.
2. Baeg EH, Kim YB, Huh K, Mook-Jung I, Kim HT, Jung MW (2003) Dynamics of population code for working memory in the prefrontal cortex. Neuron 40:177-188.
3. Batuev AS, Kursina NP, Shutov AP (1990) Unit activity of the medial wall of the frontal cortex during delayed performance in rats. Behav Brain Res 41:95-102.
4. Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:4320-4324.
5. Bower MR, Euston DR, McNaughton BL (2005) Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 25:1313-1323.
6. Chaillan FA, Marchetti E, Delfosse F, Roman FS, Soumireu-Mourat B (1997) Opposite effects depending on learning and memory demands in dorsomedial prefrontal cortex lesioned rats performing an olfactory task. Behav Brain Res 82:203-212.
7. Chang JY, Janak PH, Woodward DJ (1998) Comparison of mesocorticolimbic neuronal responses during cocaine and heroin self-administration in freely moving rats. J Neurosci 18:3098-3115.
8. Chang JY, Chen L, Luo F, Shi LH, Woodward DJ (2002) Neuronal responses in the frontal cortico-basal ganglia system during delayed matching-to-sample task: ensemble recording in freely moving rats. Exp Brain Res 142:67-80.
9. Chiba AA, Kesner RP, Reynolds AM (1994) Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. Behav Neural Biol 61:123-131.
10. Chiba AA, Kesner RP, Gibson CJ (1997) Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex. Learn Mem 4:311-317.
11. Chudasama Y, Muir JL (1997) A behavioural analysis of the delayed nonmatching to position task: the effects of scopolamine, lesions of the fornix and of the prelimbic region on mediating behaviours by rats. Psychopharmacology (Berl) 134:73-82.
12. Delatour B, Gisquet-Verrier P (1996) Prelimbic cortex specific lesions disrupt delayed-variable response tasks in the rat. Behav Neurosci 110:1282-1298.
13. Delatour B, Gisquet-Verrier P (2001) Involvement of the dorsal anterior cingulate cortex in temporal behavioral sequencing: subregional analysis of the medial prefrontal cortex in rat. Behav Brain Res 126:105-114.
14. Dias R, Aggleton JP (2000) Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 12:4457-4466.
15. Dietrich A, Allen JD (1998) Functional dissociation of the prefrontal cortex and the hippocampus in timing behavior. Behav Neurosci 112:1043-1047.
16. Fuster JM (1997) The prefrontal cortex: anatomy, physiology, and neuropsychology of the frontal lobe, Ed 3. Philadelphia: Lippincott-Raven.
17. Fuster JM (2001) The prefrontal cortex - an update: time is of the essence. Neuron 30:319-333.
18. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145-177.
19. Gisquet-Verrier P, Delatour B (2006) The role of the rat prelimbic/infralimbic cortex in working memory: not involved in the short-term maintenance but in monitoring and processing functions. Neuroscience 141:585-596.
20. Gomez Beldarrain M, Grafman J, Pascual-Leone A, Garcia-Monco JC (1999) Procedural learning is impaired in patients with prefrontal lesions. Neurology 52:1853-1860.
21. Gomez Beldarrain M, Grafman J, Ruiz de Velasco I, Pascual-Leone A, Garcia-Monco C (2002) Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks. Exp Brain Res 142:529-538.
22. Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1996) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16:823-835.
23. Hebb DO (1949) The organization of behavior; a neuropsychological theory. New York: Wiley.
24. Heidbreder CA, Groenewegen HJ (2003) The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev 27:555-579.
25. Hok V, Save E, Lenck-Santini PP, Poucet B (2005) Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc Natl Acad Sci USA 102:4602-4607.
26. Honda M, Deiber M-P, Ibanez V, Pascual-Leone A, Zhuang P, Hallett M (1998) Dynamic cortical involvement in implicit and explicit motor sequence learning: a PET study. Brain 121:2159-2173.
27. Joel D, Weiner I, Feldon J (1997) Electrolytic lesions of the medial prefrontal cortex in rats disrupt performance on an analog of the Wisconsin Card Sorting Test, but do not disrupt latent inhibition: implications for animal models of schizophrenia. Behav Brain Res 85:187-201.
28. Jung MW, Qin Y, McNaughton BL, Barnes CA (1998) Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8:437-450.
29. Kesner RP (2000) Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology 28:219-228.
30. Kesner RP, Holbrook T (1987) Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 25:653-664.
31. Lashley KS (1951) The problem of serial order in behavior. In: Cerebral mechanisms in behavior (Jeffress LA, ed), pp 112-136. New York: Wiley.
32. Liebman JM, Cooper SJ (1989) The neuropharmacological basis of reward. Oxford: Claredon.
33. McNaughton BL, Barnes CA, O'Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41-49.
34. Minai AA, Barrows GL, Levy WB (1994) Disambiguation of pattern sequences with recurrent networks. In: World Congress on Neural Networks: Proceedings of the International Neural Network Society, Vol IV, pp 178-181. Mahwah, NJ: Erlbaum.
35. Mogensen J, Holm S (1994) The prefrontal cortex and variants of sequential behaviour indications of functional differentiation between subdivisions of the rat's prefrontal cortex. Behav Brain Res 63:89-100.
36. Mulder AB, Nordquist R, Orgut O, Pennartz CM (2000) Plasticity of neuronal firing in deep layers of the medial prefrontal cortex in rats engaged in operant conditioning. Prog Brain Res 126:287-301.
37. Olds J, Milner P (1954) Positive and reinforcement produced by electrical stimulation of septal and other regions of the rat brain. J Comp Physiol Psychol 47:419-427.
38. Olds ME, Fobes JL (1981) The central basis of motivation: intracranial self-stimulation studies. Annu Rev Psychol 32:523-574.
39. Olton DS (1989) Frontal cortex, timing and memory. Neuropsychologia 27:121-130.
40. Pascual-Leone A, Wassermann EM, Grafman J, Hallett M (1996) The role of the dorsolateral prefrontal cortex in implicit procedural learning. Exp Brain Res 107:479-485.
41. Paxinos G, Watson C (1997) The rat brain, Ed 3. San Diego: Academic.
42. Pratt WE, Mizumori SJ (2001) Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task. Behav Brain Res 123:165-183.
43. Preuss TM (1995) Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J Cogn Neurosci 7:1-24.
44. Ragozzino ME, Adams S, Kesner RP (1998) Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav Neurosci 112:293-303.
45. Ragozzino ME, Wilcox C, Raso M, Kesner RP (1999) Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113:32-41.
46. Ragozzino ME, Kim J, Hassert D, Minniti N, Kiang C (2003) The contribution of the rat prelimbic-infralimbic areas to different forms of task switching. Behav Neurosci 117:1054-1065.
47. Sakurai Y, Sugimoto S (1986) Multiple unit activity of prefrontal cortex and dorsomedial thalamus during delayed go/no-go alternation in the rat. Behav Brain Res 20:295-301.
48. Sanchez-Santed F, de Bruin JP, Heinsbroek RP, Verwer RW (1997) Spatial delayed alternation of rats in a T-maze: effects of neurotoxic lesions of the medial prefrontal cortex and of T-maze rotations. Behav Brain Res 84:73-79.
49. Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063-1073.
50. Shimamura AP, Janowsky JS, Squire LR (1990) Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia 28:803-813.
51. Takehara K, Kawahara S, Kirino Y (2003) Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci 23:9897-9905.
52. Uylings HBM, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146:3-17.
53. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science [Erratum (1994) 264:16] 261:1055-1058.
54. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679.