The Eyes Have It: Hippocampal Activity Predicts Expression of Memory in Eye Movements
Open accessAbstract
Although there is widespread agreement that the hippocampus is critical for explicit episodic memory retrieval, it is controversial whether this region can also support indirect expressions of relational memory when explicit retrieval fails. Here, using functional magnetic resonance imaging (fMRI) with concurrent indirect, eye-movement-based memory measures, we obtained evidence that hippocampal activity predicted expressions of relational memory in subsequent patterns of viewing, even when explicit, conscious retrieval failed. Additionally, activity in the lateral prefrontal cortex and functional connectivity between the hippocampus and prefrontal cortex were greater for correct than for incorrect trials. Together, these results suggest that hippocampal activity can support the expression of relational memory even when explicit retrieval fails and that recruitment of a broader cortical network may be required to support explicit associative recognition.
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Prefrontal cortex executive functions mediate processing of anticipatory aspects of behavior and, with the hippocampus, regulate implementation of anticipated memory retrieval and allocation of relevance and expectancies to a memory.
“Prefrontal cortex executive functions mediate the processing of anticipatory aspects of behavior and, in collaboration with the hippocampus, these prefrontal regions also regulate the implementation of anticipated memory retrieval as well as the allocation of relevance and expectancies to a memory (219, 511, 820, 938).”
From About Sleep's Role in Memory (2013) · cites this paper as [511]
The Results report prefrontal activity during the scene cue and increased prefrontal–hippocampal connectivity during accurate associative recognition. The Discussion suggests that prefrontal regions may use hippocampally retrieved information to guide memory decisions. These passages do not establish that prefrontal executive functions mediate anticipatory behavior or allocate relevance and expectancies to a memory; the paper's interpretation is also more tentative than the claim. Page numbers are unavailable in our copy. (LLM, conf=0.85)
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Cites
Medial temporal lobe activity during source retrieval reflects information type, not memory strength
Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21335 · Cited by 191 · see citing works
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Research works printed but not linked: 35
- Aggleton JP Brown MW Episodic memory, amnesia, and the hippocampal-anterior thalamic axis Behav Brain Sci 1999 22 425 444 11301518
- Aguirre GK Zarahn E D’Esposito M The variability of human BOLD hemodynamic responses Neuroimage 1998 8 360 369 9811554
- Chun MM Phelps EA Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage Nat Neurosci 1999 2 844 847 10461225
- Cohen NJ Squire LR Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that Science 1980 210 207 210 7414331
- Davachi L Item, context, and relational episodic encoding in humans Curr Opin Neurobiol 2006 16 693 700 17097284
- Degonda N Mondadori CR Bosshardt S Schmidt CF Boesiger P Nitsch RM Hock C Henke K Implicit associative learning engages the hippocampus and interacts with explicit associative learning Neuron 2005 46 505 520 15882649
- Desjardins AE Kiehl KA Liddle PF Removal of confounding effects of global signal in functional MRI analyses Neuroimage 2001 13 751 758 11305902
- Dobbins IG Sanghoon H Cue-versus probe-dependent prefrontal cortex activity during contextual remembering J Cogn Neuro 2006 18 1439 1452 16989546
- Duarte A Ranganath C Knight RT Effects of unilateral prefrontal lesions on familiarity, recollection, and source memory J Neurosci 2005 25 8333 8337 16148241 PMC6725547
- Eichenbaum H Conscious awareness, memory and the hippocampus Nat Neurosci 1999 2 775 776 10461210
- Eichenbaum H Yonelinas AP Ranganath C The medial temporal lobe and recognition memory Annu Rev Neurosci 2007 30 123 152 17417939 PMC2064941
- Fletcher PC Henson RN Frontal lobes and human memory: insights from functional neuroimaging Brain 2001 124 849 881 11335690
- Greene AJ Gross WL Elsinger CL Rao SM An fMRI analysis of the human hippocampus: inference, context, and awareness J Cogn Neurosci 2006 18 1156 1173 16839289 PMC2078243
- Greene AJ Gross WL Elsinger CL Rao SM Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task Learn Mem 2007 14 548 553 17690338 PMC2078244
- Hannula DE Ryan JD Tranel D Cohen NJ Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia J Cogn Neuro 2007 19 1690 1705 17854282
- Hayhoe M Bensinger DG Ballard DH Task constraints in visual working memory Vision Research 1998 38 125 137 9474383
- Henderson JM Hollingworth A Eye movements and visual memory: Detecting changes to saccade targets in scenes Percept Psychophys 2003 65 58 71 12699309
- Henson RN A mini-review of fMRI studies of human medial temporal lobe activity associated with recognition memory Q J Exp Psychol, Series B 2005 58 340 360 16194973
- Holm L Eriksson J Andersson L Looking as if you know: Systematic object inspection precedes object recognition Journal of Vision 2008 8 14.1 7 18484853
- Insausti R Juottonen K Soininen H Insausti AM Partanen PV Laakso MP Pitkanen A MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices American Journal of Neuroradiology 1998 19 659 671 9576651 PMC8337393
- Manns JR Squire Perceptual learning, awareness, and the hippocampus Hippocampus 2001 11 776 782 11811672
- Moscovitch M Recovered consciousness: a hypothesis concerning modularity and episodic memory Journal of Clinical Experimental Neuropsychology 1995 17 276 290 7629272
- Moscovitch M The hippocampus as a “stupid” domain-specific module: Implications for theories of recent and remote memory, and of imagination Can J Exp Psychol 2008 62 62 79 18473631
- Preston AR Gabrieli JD Dissociation between explicit memory and configural memory in the human medial temporal lobe Cereb Cortex 2008 18 2192 2207 18234685 PMC2733308
- Ranganath C Johnson MK D’Esposito M Left anterior prefrontal activation increases with demands to recall specific perceptual information J Neurosci 2000 20 1 5 11069977 PMC6773176
- Richmond J Nelson CA Relational memory during infancy: evidence from eye tracking Developmental Science 2009 Advance Online Publication 19635082
- Rissman J Gazzaley A D’Esposito M Measuring functional connectivity during distinct stages of a cognitive task Neuroimage 2004 23 752 763 15488425
- Ryan JD Althoff RR Whitlow S Cohen NJ Amnesia is a deficit in relational memory Psychol Sci 2000 11 454 461 11202489
- Ryan JD Hannula DE Cohen NJ The obligatory effects of memory on eye movements Memory 2007 15 508 525 17613794
- Schendan HE Searl MM Melrose RJ Stern CE An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning Neuron 2003 37 1013 1025 12670429
- Smith CN Hopkins RO Squire LR Experience-dependent eye movements, awareness, and hippocampus-dependent memory J Neurosci 2006 26 11304 11312 17079658 PMC2424210
- Squire LR Stark CE Clark RE The medial temporal lobe Annu Rev Neurosci 2004 27 279 306 15217334
- Tulving E Schacter DL Priming and human memory systems Science 1990 247 301 306 2296719
- Yonelinas AP The nature of recollection and familiarity: A review of 30 years of research Journal of Memory and Language 2002 46 441 517
- Zarahn E Aguirre G D’Esposito M A trial-based experimental design for fMRI Neuroimage 1997 6 122 138 9299386
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“Prefrontal cortex executive functions mediate the processing of anticipatory aspects of behavior and, in collaboration with the hippocampus, these prefrontal regions also regulate the implementation of anticipated memory retrieval as well as the allocation of relevance and expectancies to a memory (219, 511, 820, 938).”
BackgroundEpisodic memory and beyond: the hippocampus and neocortex in transformation
Moscovitch, M., Cabeza, R., Winocur, G., & Nadel, L. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143733 · Cited by 1,062 · see citing works
Viewpoints: how the hippocampus contributes to memory, navigation and cognition
Lisman, J., Buzsáki, G., Eichenbaum, H., Nadel, L., Ranganath, C., & Redish, A. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4661 · Cited by 851 · see citing works
System consolidation of memory during sleep
Born, J., & Wilhelm, I. (2012) · Psychological Research · doi:10.1007/s00426-011-0335-6 · Cited by 667 · see citing works
Shaping of Object Representations in the Human Medial Temporal Lobe Based on Temporal Regularities
Schapiro, A. C., Kustner, L. V., & Turk-Browne, N. B. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.056 · Cited by 430 · see citing works
Sleep selectively enhances memory expected to be of future relevance
Wilhelm, I., Diekelmann, S., Molzow, I., Ayoub, A., Mölle, M., & Born, J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3575-10.2011 · Cited by 397 · see citing works
Ranganath, C. (2010) · Hippocampus · doi:10.1002/hipo.20852 · Cited by 375 · see citing works
Self-citationConscious and Unconscious Memory Systems
Squire, L. R., & Dede, A. J. O. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021667 · Cited by 366 · see citing works
Worth a glance: Using eye movements to investigate the cognitive neuroscience of memory.
Hannula, D. E. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00166 · Cited by 326 · see citing works
Blumenfeld, R. S., Parks, C. M., Yonelinas, A. P., & Ranganath, C. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21459 · Cited by 209 · see citing works
Self-citationMechanisms for widespread hippocampal involvement in cognition.
Shohamy, D., & Turk-Browne, N. B. (2013) · Journal of Experimental Psychology: General · doi:10.1037/a0034461 · Cited by 187 · see citing works
Memory Systems, Processing Modes, and Components: Functional Neuroimaging Evidence
Cabeza, R., & Moscovitch, M. (2013) · Perspectives on Psychological Science · doi:10.1177/1745691612469033 · Cited by 163 · see citing works
Cognitive impairments in psychotic disorders: common mechanisms and measurement
Barch, D. M., & Sheffield, J. M. (2014) · World Psychiatry · doi:10.1002/wps.20145 · Cited by 154 · see citing works
Generalization of value in reinforcement learning by humans
Wimmer, G. E., Daw, N. D., & Shohamy, D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08017.x · Cited by 111 · see citing works
Monti, J. M., Hillman, C. H., & Cohen, N. J. (2012) · Hippocampus · doi:10.1002/hipo.22023 · Cited by 95 · see citing works
How the Brain’s Navigation System Shapes Our Visual Experience
Nau, M., Julian, J. B., & Doeller, C. F. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.06.008 · Cited by 79 · see citing works
Wang, J. X., Cohen, N. J., & Voss, J. L. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.04.003 · Cited by 75 · see citing works
Common Priority Map for Selection History, Reward and Emotion in the Oculomotor System
Belopolsky, A. V. (2015) · Perception · doi:10.1177/0301006615596866 · Cited by 42 · see citing works
A review of autobiographical memory studies on patients with schizophrenia spectrum disorders
Zhang, Y., Kuhn, S. K., Jobson, L., & Haque, S. (2019) · BMC Psychiatry · doi:10.1186/s12888-019-2346-6 · Cited by 35 · see citing works
- Authors
- Hannula, D. E., & Ranganath, C.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- Hannula, Deborah E.
- ORCID
- Hannula, Deborah E.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2009-09
- Volume
- 63
- Issue
- 5
- Pages
- 592-599
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2747814
- OpenAlex
- W2133280872
- Cited by
- 352
- References
- 1
- Citations by year
- 2026: 17 · 2025: 14 · 2024: 20 · 2023: 13 · 2022: 11 · 2021: 14 · 2020: 25 · 2019: 30 · 2018: 26 · 2017: 44 · 2016: 22 · 2015: 26 · 2014: 25 · 2013: 17 · 2012: 22
- FWCI
- 7.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- University of California, Davis
- National Institute of Mental Health (F32MH075513, R01MH068721, MH68721)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- hippocampus, relational memory, eye movements, eye tracking, lateral prefrontal cortex, associative recognition memory
- MeSH terms
- Analysis of Variance, Association Learning, Cues, Eye Movements, Face, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Memory, Neural Pathways, Neuropsychological Tests, Photic Stimulation, Reaction Time, Temporal Lobe, Time Factors, Prefrontal Cortex, Recognition, Psychology, Eye Movement Measurements
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