Layer V perirhinal cortical ensemble activity during object exploration: A comparison between young and aged rats

Hippocampus

Volumn 22, Issue 10, 2012, Pages 2080-2093

  Burke, S N ^a,b   Hartzell, A L ^a,b   Lister, J P ^a,b   Hoang, L T ^a,b   Barnes, C A ^a,b,c,d  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c University of Arizona   (United States)

^d UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Immediate early gene; Object field; Object recognition; Rat

Indexed keywords

RNA;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; NERVE CELL; NONHUMAN; PERIRHINAL CORTEX; PRIORITY JOURNAL; RAT; RECOGNITION; TASK PERFORMANCE; VISUAL MEMORY;

AGE FACTORS; AGING; ANIMALS; CEREBRAL CORTEX; EXPLORATORY BEHAVIOR; MAZE LEARNING; NEURONS; RATS; RATS, INBRED F344; RECOGNITION (PSYCHOLOGY);

EID: 84866334849     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22066     Document Type: Article

References (55)

1. Aggleton JP, Kyd RJ, Bilkey DK. 2004. When is the perirhinal cortex necessary for the performance of spatial memory tasks? Neurosci Biobehav Rev 28: 611-624.
2. Barnes CA, Rao G, McNaughton BL. 1996. Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats. Learn Mem 3(2-3): 124-137.
3. Barnes CA, Suster MS, Shen J, McNaughton BL. 1997. Multistability of cognitive maps in the hippocampus of old rats. Nature 388: 272-275.
4. Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ. 2007. Perceptual functions of perirhinal cortex in rats: Zero-delay object recognition and simultaneous oddity discriminations. J Neurosci 27: 2548-2559.
5. Brown MW, Aggleton JP. 2001. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51-61.
6. Bucci DJ, Phillips RG, Burwell RD. 2000. Contributions of postrhinal and perirhinal cortex to contextual information processing. Behav Neurosci 114: 882-894.
7. Burke SN, Chawla MK, Penner MR, Crowell BE, Worley PF, Barnes CA, McNaughton BL. 2005. Differential encoding of behavior and spatial context in deep and superficial layers of the neocortex. Neuron 45: 667-674.
8. Burke SN, Ryan L, Barnes CA. 2012. Characterizing cognitive aging of recognition memory and related processes in animal models and in humans. Frontiers Aging Neuroscience, in press.
9. Burke SN, Wallace JL, Nematollahi S, Uprety AR, Barnes CA. 2010. Pattern separation deficits may contribute to age-associated recognition impairments. Behav Neurosci 124: 559-573.
10. Burke SN, Wallace JL, Hartzell AL, Nematollahi S, Plange K, Barnes CA. 2011 Age-associated deficits in pattern separation functions of the perirhinal cortex: A cross-species consensus. Behavioral Neuroscience 125: 836-847.
11. Burke SN, Maurer AP, Hartzell AL, Nematollahi S, Uprety AR, Wallace JL, Barnes CA. 2012. Representation of three-dimensional objects by the rat perirhinal cortex. Hippocampus 22: 2032-2044.
12. Burwell RD. 2001. Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat. J Comp Neurol 437: 17-41.
13. Burwell RD, Amaral DG. 1998. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391: 293-321.
14. Burwell RD, Saddoris MP, Bucci DJ, Wiig KA. 2004. Corticohippocampal contributions to spatial and contextual learning. J Neurosci 24: 3826-3836.
15. Chawla MK, Lin G, Olson K, Vazdarjanova A, Burke SN, McNaughton BL, Worley PF, Guzowski JF, Roysam B, Barnes CA. 2004. 3D-catFISH: A system for automated quantitative three-dimensional compartmental analysis of temporal gene transcription activity imaged by fluorescence in situ hybridization. J Neurosci Methods 139: 13-24.
16. Cole AJ, Saffen DW, Baraban JM, Worley PF. 1989. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340: 474-476.
17. Desimone R. 1996. Neural mechanisms for visual memory and their role in attention. Proc Natl Acad Sci USA 93: 13494-13499.
18. Edling Y, Ingelman-Sundberg M, Simi A. 2007. Glutamate activates c-fos in glial cells via a novel mechanism involving the glutamate receptor subtype mGlu5 and the transcriptional repressor DREAM. Glia 55: 328-340.
19. Erickson CA, Jagadeesh B, Desimone R. 2000. Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys. Nat Neurosci 3: 1143-1148.
20. Fletcher BR, Calhoun ME, Rapp PR, Shapiro ML. 2006. Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity. J Neurosci 26: 1507-1515.
21. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behav Neurosci 107: 618-626.
22. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA. 2000. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
23. Guzowski JF, McNaughton BL, Barnes CA, Worley PF. 1999. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2: 1120-1124.
24. Guzowski JF, McNaughton BL, Barnes CA, Worley PF. 2001. Imaging neural activity with temporal and cellular resolution using FISH. Curr Opin Neurobiol 11: 579-584.
25. Guzowski JF, Miyashita T, Chawla MK, Sanderson J, Maes LI, Houston FP, Lipa P, McNaughton BL, Worley PF, Barnes CA. 2006. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc Natl Acad Sci USA 103: 1077-1082.
26. Kent BA, Brown TH. 2012 Dual functions of perirhinal cortex in fear conditioning. Hippocampus 22: 2068-2079.
27. Liu P, Gupta N, Jing Y, Zhang H. 2008. Age-related changes in polyamines in memory-associated brain structures in rats. Neuroscience 155: 789-796.
28. Liu P, Jing Y, Zhang H. 2009. Age-related changes in arginine and its metabolites in memory-associated brain structures. Neuroscience 164: 611-628.
29. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF. 1995. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14: 433-445.
30. Machin P, Vann SD, Muir JL, Aggleton JP. 2002. Neurotoxic lesions of the rat perirhinal cortex fail to disrupt the acquisition or performance of tests of allocentric spatial memory. Behav Neurosci 116: 232-240.
31. McNaughton BL, Morris RG. 1987. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10: 408-415.
32. McTighe SM, Cowell RA, Winters BD, Bussey TJ, Saksida LM. 2010. Paradoxical false memory for objects after brain damage. Science 330: 1408-1410.
33. Morgan JI, Cohen DR, Hempstead JL, Curran T. 1987. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192-197.
34. Moyer JR, Jr., Furtak SC, McGann JP, Brown TH. 2009. Aging-related changes in calcium-binding proteins in rat perirhinal cortex. Neurobiol Aging 32: 1693-1706.
35. Norman G, Eacott MJ. 2005. Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav Neurosci 119: 557-566.
36. O'Keefe J, Conway DH. 1978. Hippocampal place units in the freely moving rat: Why they fire where they fire. Exp Brain Res 31: 573-590.
37. Piterkin P, Cole E, Cossette MP, Gaskin S, Mumby DG. 2008. A limited role for the hippocampus in the modulation of novel-object preference by contextual cues. Learn Mem 15: 785-791.
38. Rapp PR, Deroche PS, Mao Y, Burwell RD. 2002. Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. Cereb Cortex 12: 1171-1179.
39. Rosi S, Vazdarjanova A, Ramirez-Amaya V, Worley PF, Barnes CA, Wenk GL. 2006. Memantine protects against LPS-induced neuroinflammation, restores behaviorally-induced gene expression and spatial learning in the rat. Neuroscience 142: 1303-1315.
40. Shen J, Barnes CA, Wenk GL, McNaughton BL. 1996. Differential effects of selective immunotoxic lesions of medial septal cholinergic cells on spatial working and reference memory. Behav Neurosci 110: 1181-1186.
41. Thome A, Erickson C, Lipa P, Barnes CA. 2012. Differential effects of experience on tuning properties of macaque MTL neurons in a passive viewing task, Hippocampus, this issue.
42. Toner CK, Pirogovsky E, Kirwan CB, Gilbert PE. 2009. Visual object pattern separation deficits in nondemented older adults. Learn Mem 16: 338-342.
43. Vazdarjanova A, Guzowski JF. 2004. Differences in hippocampal neuronal population responses to modifications of an environmental context: Evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24: 6489-6496.
44. Vazdarjanova A, Ramirez-Amaya V, Insel N, Plummer TK, Rosi S, Chowdhury S, Mikhael D, Worley PF, Guzowski JF, Barnes CA. 2006. Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498: 317-329.
45. Wan H, Aggleton JP, Brown MW. 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19: 1142-1148.
46. Warburton EC, Glover CP, Massey PV, Wan H, Johnson B, Bienemann A, Deuschle U, Kew JN, Aggleton JP, Bashir ZI, et al. 2005. cAMP responsive element-binding protein phosphorylation is necessary for perirhinal long-term potentiation and recognition memory. J Neurosci 25: 6296-6303.
47. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
48. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261: 1055-1058.
49. Winters BD, Bussey TJ. 2005. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25: 52-61.
50. Woloszyn L, Sheinberg DL. 2012. Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex. Neuron 74: 193-205.
51. Xiang JZ, Brown MW. 1998. Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37(4-5): 657-676.
52. Zhu XO, Brown MW. 1995. Changes in neuronal activity related to the repetition and relative familiarity of visual stimuli in rhinal and adjacent cortex of the anaesthetised rat. Brain Res 689: 101-110.
53. Zhu XO, Brown MW, Aggleton JP. 1995a. Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur J Neurosci 7: 753-765.
54. Zhu XO, Brown MW, McCabe BJ, Aggleton JP. 1995b. Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience 69: 821-829.
55. Zhu XO, McCabe BJ, Aggleton JP, Brown MW. 1997. Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment. Neurosci Lett 229: 141-143.