Dissociated signals in human dentate gyrus and CA3 predict different facets of recognition memory

Journal of Neuroscience

Volumn 34, Issue 40, 2014, Pages 13301-13313

  Reagh, Zachariah M ^a,b   Watabe, Joseph ^c   Ly, Maria ^c   Murray, Elizabeth ^a,b   Yassa, Michael A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

CA3; Dentate; fMRI; Hippocampus; Memory; Recognition

Indexed keywords

ARTICLE; DENTATE GYRUS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPAL CA3 REGION; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; MEMORY CONSOLIDATION; PATTERN RECOGNITION; REACTION TIME; RECOGNITION; REPETITION PRIMING; TASK PERFORMANCE; ADULT; ANALYSIS OF VARIANCE; BLOOD; FACE; FEMALE; HEMISPHERIC DOMINANCE; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADULT; ANALYSIS OF VARIANCE; CA3 REGION, HIPPOCAMPAL; DENTATE GYRUS; FACE; FEMALE; FUNCTIONAL LATERALITY; HEALTHY VOLUNTEERS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REACTION TIME; RECOGNITION (PSYCHOLOGY); YOUNG ADULT;

EID: 84907494800     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2779-14.2014     Document Type: Article

References (48)

1. Aggleton JP, Wright NF, Vann SD, Saunders RC (2012) Medial temporal lobe projections to the retrosplenial cortex of the macaque monkey. Hip-pocampus 22:1883-1900.CrossRef Medline
2. Avants BB, Tustison N, Song G (2009) Advanced normalization tools (ANTS). Philadelphia: Penn Image Computing and Science Laboratory; University of Pennsylvania.
3. Bakker A, Kirwan CB, Miller M, Stark CEL (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-1642.CrossRef Medline
4. Barker GRI, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31:10721-10731.CrossRef Medline
5. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10:433-436.Medline
6. Brown MW, Aggleton JP (2001) Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51-61.CrossRef Medline
7. Brown MW, Bashir ZI (2002) Evidence concerning how neurons of the perirhinal cortex may affect familiarity discrimination. Philos Trans R Soc Lond B Biol Sci 357:1083-1095.CrossRef Medline
8. Buffalo EA, Reber PJ, Squire LR (1998) The human perirhinal cortex and recognition memory. Hippocampus 8:330-339.CrossRef Medline
9. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853-8860.Medline
10. Cox RW (1996) AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173.CrossRef Medline
11. Daselaar SM, Fleck MS, Cabeza R (2006) Triple dissociation in the medial temporal lobes: Recollection, familiarity, and novelty. J Neurophysiol 96: 1902-1911.CrossRef Medline
12. Diana RA, Yonelinas AP, Ranganath C (2007) Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends Cogn Sci 11:379-386.CrossRef Medline
13. Diana RA, Yonelinas AP, Ranganath C (2012) Adaptation to cognitive context and item information in the medial temporal lobes. Neuropsychologia 50:3062-3069.CrossRef Medline
14. Duncan K, Curtis C, Davachi L (2009) Distinct memory signatures in the hippocampus: Intentional states distinguish match and mismatch enhancement signals. J Neurosci 29:131-139.CrossRef Medline
15. Duncan K, Ketz N, Inati SJ, Davachi L (2012) Evidence for area CA1 as a match/mismatch detector: A high-resolution fMRI study of the human hippocampus. Hippocampus 22:389-398.CrossRef Medline
16. Duvernoy H (1998) The human hippocampus: Functional anatomy, vascularization, and serial sections with MRI. Berlin: Springer.
17. Düzel E, Vargha-Khadem F, Heinze HJ, Mishkin M (2001) Brain activity evidence for recognition without recollection after early hippocampal damage. Proc Natl Acad Sci U S A 98:8101-8106.CrossRef Medline
18. Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123-152.CrossRef Medline
19. Fortin NJ, Wright SP, Eichenbaum H (2004) Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431:188-191.CrossRef Medline
20. Hannula DE, Ranganath C (2008) Medial temporal lobe activity predicts successful relational memory binding. J Neurosci 28:116-124.CrossRef Medline
21. Haskins AL, Yonelinas AP, Quamme JR, Ranganath C (2008) Perirhinal cortex supports encoding and familiarity-based recognition of novel associations. Neuron 59:554-560.CrossRef Medline
22. Johnson JD, Rugg MD (2007) Recollection and the reinstatement of encoding-related cortical activity. Cereb Cortex 17:2507-2515.CrossRef Medline
23. Johnson JD, McDuff SGR, Rugg MD, Norman KA (2009) Recollection, familiarity, and cortical reinstatement: A multivoxel pattern analysis. Neuron 63:697-708.CrossRef Medline
24. Jutras MJ, Buffalo EA (2010) Recognition memory signals in the macaque hippocampus. Proc Natl Acad Sci U S A 107:401-406.CrossRef Medline
25. Kobayashi Y, Amaral DG (2003) Macaque monkey retrosplenial cortex: II. Cortical afferents. J Comp Neurol 446:48-79.CrossRef Medline
26. Kobayashi Y, Amaral DG (2007) Macaque monkey retrosplenial cortex: III. Cortical efferents. J Comp Neurol 502:810-833.CrossRef Medline
27. Kumaran D, Maguire EA (2006) An unexpected sequence of events: Mismatch detection in the human hippocampus. PLoS Biol 4:e424.CrossRef Medline
28. Kumaran D, Maguire EA (2007) Match mismatch processes underlie human hippocampal responses to associative novelty. J Neurosci 27:8517-8524.CrossRef Medline
29. Lacy JW, Yassa MA, Stark SM, Muftuler LT, Stark CE (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.CrossRef Medline
30. LaRocque KF, Smith ME, Carr VA, Witthoft N, Grill-Spector K, Wagner AD (2013) Global similarity and pattern separation in the human medial temporal lobe predict subsequent memory. J Neurosci 33:5466-5474.CrossRef Medline
31. Lisman JE (1999) Relating hippocampal circuitry to function: Recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22: 233-242.CrossRef Medline
32. Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR (2003) Recognition memory and the human hippocampus. Neuron 37:171-180.CrossRef Medline
33. Murray EA, Bussey TJ (1999) Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn Sci 3:142-151.CrossRef Medline
34. Murray EA, Baxter MG, Gaffan D (1998) Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. Behav Neurosci 112:1291-1303.CrossRef Medline
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.CrossRef Medline
36. Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230-240.CrossRef Medline
37. Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13:713-726.CrossRef Medline
38. Reagh ZM, Yassa MA (2014) Repetition strengthens target recognition but impairs similar lure discrimination: Evidence for trace competition. Learn Mem 21:342-346.CrossRef Medline
39. Staresina BP, Duncan KD, Davachi L (2011) Perirhinal and parahippocampal cortices differentially contribute to later recollection of object-and scene-related event details. J Neurosci 31:8739-8747.CrossRef Medline
40. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430-2451.Medline
41. Vilberg KL, Rugg MD (2012) The neural correlates of recollection: Transient versus sustained FMRI effects. J Neurosci 32:15679-15687.CrossRef Medline
42. Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hip-pocampus and perirhinal cortex to recognition memory. J Neurosci 19: 1142-1148.Medline
43. Wyss JM, Van Groen T (1992) Connections between the retrosplenial cor tex and the hippocampal formation in the rat: A review. Hippocampus 2:1-11.CrossRef Medline
44. Yassa MA, Stark CEL (2008) Multiple signals of recognition memory in the medial temporal lobe. Hippocampus 18:945-954.CrossRef Medline
45. Yassa MA, Stark CEL (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515-525.CrossRef Medline
46. Yonelinas AP, Kroll NEA, Quamme JR, Lazzara MM, Sauvé MJ, Widaman KF, Knight RT (2002) Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5:1236-1241.CrossRef Medline
47. Yonelinas AP, Otten LJ, Shaw KN, Rugg MD (2005) Separating the brain regions involved in recollection and familiarity in recognition memory. J Neurosci 25:3002-3008.CrossRef Medline
48. Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA (1989) Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci 9:4355-4370.Medline