Spatial discrimination deficits as a function of mnemonic interference in aged adults with and without memory impairment

Hippocampus

Volumn 24, Issue 3, 2014, Pages 303-314

  Reagh, Zachariah M ^a   Roberts, Jared M ^a   Ly, Maria ^a   Diprospero, Natalie ^a   Murray, Elizabeth ^a   Yassa, Michael A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Hippocampus; Interference; Neurocognitive aging; Pattern separation; Spatial discrimination

Indexed keywords

ADULT; AGED; AGING; ARTICLE; COGNITIVE DEFECT; EARLY DIAGNOSIS; FEMALE; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MNEMONIC INTERFERENCE; NEUROPSYCHOLOGICAL TEST; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RECALL; REY AUDITORY VERBAL LEARNING TEST; SPATIAL DISCRIMINATION; SPATIAL MEMORY; TASK PERFORMANCE; YOUNG ADULT;

HIPPOCAMPUS; INTERFERENCE; NEUROCOGNITIVE AGING; PATTERN SEPARATION; SPATIAL DISCRIMINATION;

ADULT; AGED; AGING; DISCRIMINATION (PSYCHOLOGY); DISCRIMINATION LEARNING; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MEMORY DISORDERS; MEMORY, EPISODIC; MENTAL RECALL; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; SPACE PERCEPTION; VERBAL LEARNING; YOUNG ADULT;

EID: 84893957687     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22224     Document Type: Article

References (54)

1. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-1642. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2829853&tool=pmcentrez&rendertype=abstract.
2. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, et al. 2012. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74:467-474. doi:10.1016/j.neuron.2012.03.023.
3. Braak H, Braak E. 1995. Staging of alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 16:271-278. doi:10.1016/0197-4580(95)00021-6.
4. Braak H, Braak E. 1996. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol Scand Suppl 165:3-12. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8740983.
5. Braak H, Braak E, Bohl J. 1993. Staging of Alzheimer-related cortical destruction. Eur Neurol 9(Suppl 1):257-261; discussion 269-272. Retrieved from http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8307060.
6. Brady TF, Konkle T, Alvarez GA, Oliva A. 2008. Visual long-term memory has a massive storage capacity for object details. Proc Natl Acad Sci USA 105:14325-14329. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2533687&tool=pmcentrez&rendertype=abstract.
7. Buckner RL, Wheeler ME. 2001. The cognitive neuroscience of remembering. Nat Rev Neurosci 2:624-634. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11533730.
8. Deshmukh SS, Knierim JJ. 2012. Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front Behav Neurosci 69. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3203372&tool=pmcentrez&rendertype=abstract.
9. Deshmukh SS, Yoganarasimha D, Voicu H, Knierim JJ. 2010. Theta modulation in the medial and the lateral entorhinal cortex. J Neurophysiol 104:994-1006. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2934945&tool=pmcentrez&rendertype=abstract.
10. Driscoll I, Howard SR, Prusky GT, Rudy JW, Sutherland RJ. 2005. Seahorse wins all races: Hippocampus participates in both linear and non-linear visual discrimination learning. Behav Brain Res 164:29-35. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16024101.
11. Eichenbaum H, Lipton PA. 2008. Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas. (Hasselmo EI Moser ME, Moser M-B, Eds.) Hippocampus 18:1314-1324. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/19021265.
12. Gallagher M, Colantuoni C, Eichenbaum H, Haberman RP, Rapp PR, Tanila H, Wilson IA. 2006. Individual differences in neurocognitive aging of the medial temporal lobe. Age (Omaha) 28:221-233. doi:10.1007/s11357-006-9017-5.
13. Gallagher M, Bizon JL, Hoyt EC, Helm KA, Lund PK. 2003. Effects of aging on the hippocampal formation in a naturally occurring animal model of mild cognitive impairment. Exp Gerontol 38:71-77. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12543263.
14. Gallagher M, Burwell RD, 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.
15. Gilbert PE, Kesner RP, Lee I. 2001. Dissociating hippocampal subregions: Double dissociation between dentate gyrus and CA1. Hippocampus 11:626-636. Retrieved from http://www.ncbi.nlm.nih. gov/pubmed/11811656.
16. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ. 2001. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 14(1 Pt 1):21-36. Retrieved from http://eprints.ucl.ac.uk/4191/.
17. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792-1794. Retrieved from http://www.ncbi.nlm. nih.gov/pubmed/15961670.
18. Holden HM, Hoebel C, Loftis K, Gilbert PE. 2012. Spatial pattern separation in cognitively normal young and older adults. Hippocampus 000. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/22467270.
19. Holland BS, Copenhaver MD. 1987. An improved sequentially rejective Bonferroni Test procedure. Biometrics 43:417-423. Retrieved from http://www.jstor.org/stable/2531823.
20. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70. doi:10.2307/4615733.
21. Hunsaker MR, Kesner RP. 2013. The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci Biobehav Rev 37:36-58. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/23043857.
22. Hunsaker MR, Rosenberg JS, Kesner RP. 2008. The role of the dentate gyrus, CA3a, b, and CA3c for detecting spatial and environmental novelty. Hippocampus 18:1064-1073. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18651615.
23. Lacy JW, Yassa MA, Stark SM, Muftuler LT, Stark CEL. 2011. Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity. Learn Mem 18:15-18. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3023966& tool=pmcentrez&rendertype=abstract.
24. Leal SL, Yassa MA. 2013. Perturbations of neural circuitry in aging, mild cognitive impairment, and Alzheimer's disease. Ageing Res Rev 12:823-831. doi:10.1016/j.arr.2013.01.006.
25. Leutgeb JK, Leutgeb S, Moser M-B, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/17303747.
26. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser M-B, et al. 2005. Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48:345-358. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16242413.
27. Leutgeb S, Leutgeb JK. 2007. Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14:745-757. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18007018.
28. Leutgeb S, Leutgeb JK, Treves A, Moser M-B, Moser EI. 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295-1298. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15272123.
29. Ly M, Murray E, Yassa MA. 2013. Perceptual versus conceptual interference and pattern separation of verbal stimuli in young and older adults. Hippocampus 000. doi:10.1002/hipo.22110.
30. Marr D. 1971. Simple memory: A theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23-81. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4399412.
31. McClelland JL, McNaughton BL, O'Reilly RC. 1995. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7624455.
32. McTighe SM, Mar AC, Romberg C, Bussey TJ, Saksida LM. 2009. A new touchscreen test of pattern separation: Effect of hippocampal lesions. NeuroReport 20:881-885. Retrieved from http://www. ncbi.nlm.nih.gov/pubmed/19421077.
33. Norman KA. 2010. How hippocampus and cortex contribute to recognition memory: Revisiting the complementary learning systems model. Hippocampus 20:1217-1227.
34. Norman KA, O'Reilly RC. 2003. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach. Psychol Rev 110:611-646. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/14599236.
35. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
36. O'Reilly RC, Norman KA. 2002. Hippocampal and neocortical contributions to memory: Advances in the complementary learning systems framework. Trends Cogn Sci 6:505-510. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12475710.
37. Peirce JW. 2007. PsychoPy-Psychophysics software in Python. J Neurosci Methods 162:8-13. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2018741&tool=pmcentrez&rendertype=abstract.
38. Peirce JW. 2008. Generating stimuli for neuroscience using psychopy. Front Neuroinf 10. doi:10.3389/neuro.11.010.2008.
39. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, et al. 2005. Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cereb Cortex 15:1676-1689. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15703252.
40. Staresina BP, Davachi L. 2009. Mind the gap: Binding experiences across space and time in the human hippocampus. Neuron 63:267-276. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/19640484.
41. Stark SM, Yassa MA, Stark CEL. 2010. Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learn Mem 17:284-288. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2884287&tool=pmcentrez&rendertype=abstract.
42. Stark SM, Yassa MA, Lacy JW, Stark CEL. 2013. A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment. Neuropsychologia 1-8. doi:10.1016/j.neuropsychologia.2012.12.014.
43. Stranahan AM, Haberman RP, Gallagher M. 2011. Cognitive decline is associated with reduced reelin expression in the entorhinal cortex of aged rats. Cereb Cortex 21:392-400. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3020582&tool=pmcentrez&rendertype=abstract.
44. Stranahan AM, Mattson MP. 2010. Selective vulnerability of neurons in layer ii of the entorhinal cortex during aging and Alzheimer's Disease. Neural Plast 2010:108190. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3039218&tool=pmcentrez&rendertype=abstract.
45. Stranahan AM, Salas-Vega S, Jiam NT, Gallagher M. 2011. Interference with reelin signaling in the lateral entorhinal cortex impairs spatial memory. Neurobiol Learn Mem 96:150-155. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21492744.
46. Treves A, Rolls ET. 1994. Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374-391. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7842058.
47. Tulving E. 2002. Episodic memory: From mind to brain. Annu Rev Psychol 53:1-25. doi:10.1146/annurev.psych.53.100901.135114.
48. van der Elst W, Boxtel MPJ, Breukelen GJP, Jolles J. 2005) Rey's verbal learning test: Normative data for 1855 healthy participants aged 24-81 years and the influence of age, sex, education, and mode of presentation. J Int Neuropsychol Soc 11:290-302.
49. Walhovd KB, Fjell AM, Dale AM, McEvoy LK, Brewer J, Karow DS, Salmon DP, et al. 2010. Multi-modal imaging predicts memory performance in normal aging and cognitive decline. Neurobiol Aging 31:1107-1121. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18838195.
50. Yang W, Ang LC, Strong MJ. 2005. Tau protein aggregation in the frontal and entorhinal cortices as a function of aging. Brain Res Dev Brain Res 156:127-138. Retrieved from http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16110532.
51. Yassa MA, Lacy JW, Stark SM, Albert MS, Gallagher M, Stark CEL. 2011. Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 21:968-979. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3010452& tool=pmcentrez&rendertype=abstract.
52. Yassa MA, Mattfeld AT, Stark SM, Stark CEL. 2011. Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proc Natl Acad Sci USA 108:8873-8878. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3102362&tool=pmcentrez&rendertype=abstract.
53. Yassa MA, Stark SM, Bakker A, Albert MS, Gallagher M, Stark CEL. 2010. High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic Mild Cognitive Impairment. NeuroImage 51:1242-1252. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2909476& tool=pmcentrez&rendertype=abstract.
54. Yassa MA, Stark CEL. 2011. Pattern separation in the hippocampus. Trends Neurosci 34:515-525. Retrieved from http://www.pubmedcentral.nih. gov/articlerender.fcgi?artid=3183227&tool=pmcentrez&rendertype= abstract.