Abstract
Several studies have begun to demonstrate that contextual memories constitute an important mechanism to guide our attention. Although there is general consensus that the hippocampus is involved in the encoding of contextual memories, it is controversial whether this structure can support implicit forms of contextual memory. Here, we combine automated segmentation of structural MRI with neurobehavioral assessment of implicit contextual memory-guided attention to test the hypothesis that hippocampal volume would predict the magnitude of implicit contextual learning. Forty healthy subjects underwent 3T magnetic resonance imaging brain scanning with subsequent automatic measurement of the total brain and hippocampal (right and left) volumes. Implicit learning of contextual information was measured using the contextual cueing task. We found that both left and right hippocampal volumes positively predicted the magnitude of implicit contextual learning. Larger hippocampal volume was associated with superior implicit contextual memory performance. This study provides compelling evidence that implicit contextual memory-guided attention is hippocampus-dependent.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acheson DT, Gresack JE, Risbrough VB (2012) Hippocampal dysfunction effects on context memory: possible etiology for posttraumatic stress disorder. Neuropharmacology 62(2):674–685
Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci 28(24):6211–6219
Aminoff E, Schacter DL, Bar M (2008) The cortical underpinnings of context-based memory distortion. J Cogn Neurosci 20:2226–2237
Aminoff E, Kveraga K, Bar M (2013) The role of the parahippocampal cortex in cognition. Trends Cogn Sci 17:379–390
Auckland ME, Cave KR, Donnelly N (2007) Nontarget objects can influence perceptual processes during object recognition. Psychon Bull Rev 14(2):332–337
Bar M, Ullman S (1996) Spatial context in recognition. Perception 25:343–352
Bar M, Aminoff E, Ishai A (2008) Famous faces activate contextual associations in the parahippocampal cortex. Cereb Cortex 18:1233–1238
Brewin CR, Kleiner JS, Vasterling JJ, Field AP (2007) Memory for emotionally neutral information in posttraumatic stress disorder: a meta-analytic investigation. J Abnorm Psychol 116(3):448–463
Buchsbaum B, D’Esposito M (2009) Repetition suppression and reactivation in auditory-verbal short-term recognition memory Cereb. Cortex 19:1474–1485
Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641
Cacciaglia R, Pohlack ST, Flor H, Nees F (2015) Dissociable roles for hippocampal and amygdalar volume in human fear conditioning. Brain Struct Funct 220:2575–2586
Chun MM, Jiang Y (1998) Contextual cueing: implicit learning and memory of visual context guides spatial attention. Cogn Psychol 36(1):28–71
Chun MM, Phelps EA (1999) Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nat Neurosci 2(9):844–847
Cohen NJ, Poldrack R, Eichenbaum H (1997) Memory for items and memory for relations in the procedural/declarative memory framework. Memory 5:131–178
Cohen NJ, Ryan J, Hunt C, Romine L, Wszalek T, Nash C (1999) Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 9(1):83–98
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9(2):179–194
Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980
Eichenbaum H, Otto T, Cohen NJ (1994) Two component functions of the hippocampal memory system. Behav Brain Sci 17:449–517
Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425(6954):184–188
Elman JA, Shimamura AP (2011) Task relevance modulates successful retrieval effects during explicit and implicit memory tests. Neuroimage 56:345–353
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601
Epstein R, Ward E (2010) How reliable are visual context effects in the parahippocampal place area? Cereb Cortex 20:294–303
Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11044–11049
Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9(2):195–207
Geyer T, Baumgartner F, Müller HJ, Pollmann S (2012) Medial temporal lobe-dependent repetition suppression and enhancement due to implicit vs. explicit processing of individual repeated search displays. Front Hum Neurosci 6:272
Giesbrecht B, Sy JL, Guerin SA (2013) Both memory and attention systems contribute to visual search for targets cued by implicitly learned context. Vis Res 85:80–89
Giovanello KS, Verfaellie M, Keane MM (2003) Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 3(3):186–194
Goldfarb EV, Chun MM, Phelps EA (2016) Memory-guided attention: independent contributions of the hippocampus and striatum. Neuron 89:317–324
Greene AJ, Gross WL, Elsinger CL, Rao SM (2007) Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task. Learn Mem 14(8):548–553
Grimm O, Pohlack S, Cacciaglia R, Winkelmann T, Plichta MM, Demirakca T, Flor H (2015) Amygdalar and hippocampal volume: a comparison between manual segmentation, Freesurfer and VBM. J Neurosci Methods 253:254–261
Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A, Dickerson B, Fischl B (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 32:180–194
Hannula DE, Greene AJ (2012) The hippocampus reevaluated in unconscious learning and memory: at a tipping point? Front Hum Neurosci 6(80):1–20
Hannula DE, Ranganath C (2009) The eyes have it: hippocampal activity predicts expression of memory in eye movements. Neuron 63:592–599
Henke K (2010) A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 11(7):523–532
Henke K, Buck A, Weber B, Wieser HG (1997) Human hippocampus establishes associations in memory. Hippocampus 7(3):249–256
Horner AJ, Gadian DG, Fuentemilla L, Jentschke S, Vargha-Khadem F et al (2012) A rapid, hippocampus-dependent, item-memory signal that initiates context memory in humans. Curr Biol 22:2369–2374
Hutchinson JB, Turk-Browne NB (2012) Memory-guided attention: control from multiple memory systems. Trends Cogn Sci 16(12):576–579
Hyman JM, Ma L, Balaguer-Ballester E, Durstewitz D, Seamans JK (2012) Contextual encoding by ensembles of medial prefrontal cortex neurons. Proc Natl Acad Sci 109(13):5086–5091
Konkel A, Cohen NJ (2009) Relational memory and the hippocampus: representations and methods. Front Neurosci 3:166–174
Kveraga K et al (2011) Early onset of neural synchronization in the contextual associations network. Proc Natl Acad Sci USA 108:3389–3394
Lang S, Kroll A, Lipinski SJ, Wessa M, Ridder S, Christmann C et al (2009) Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex. Eur J Neurosci 29(4):823–832
Lee TG, Blumenfeld RS, D’Esposito M (2013) Disruption of dorsolateral but not ventrolateral prefrontal cortex improves unconscious perceptual memories. J Neurosci 33(32):13233–13237
Manelis A, Reder LM (2012) Procedural learning and associative memory mechanisms contribute to contextual cueing: evidence from fMRI and eye-tracking. Learn Mem 9:527–534
Manelis A, Reder LM, Hanson SJ (2011) Dynamic changes in the medial temporal lobe during incidental learning of object-location associations. Cereb Cortex 22:828–837
Manginelli A, Langer N, Klose D, Pollmann S (2013) Contextual cueing under working memory load: selective interference of viuospatial load with expression of learning. Attent Percept Psychophys 75:1103–1117
Manns JR, Squire LR (2001) Perceptual learning, awareness, and the hippocampus. Hippocampus 11:776–782
Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14(6):417–428
Moscovitch M (1992) Memory and working-with-memory: a component process model based on modules and central systems. J Cogn Neurosci 4:257–267
Moscovitch M (2008) The hippocampus as a “stupid” domain-specific module: implications for theories of recent and remote memory, and of imagination. Can J Exp Pychol 62:62–79
Moscovitch M, Nadel L, Winocur G, Gilboa A, Rosenbaum RS (2006) The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr Opin Neurobiol 16:179–190
Moses SN, Ryan JD (2006) A comparison and evaluation of the predictions of relational and conjunctive accounts of hippocampal function. Hippocampus 16:43–65
Olson IR, Moore KS, Stark M, Chatterjee A (2006) Visual working memory is impaired when the medial temporal lobe is damaged. J Cogn Neurosci 18:1087–1097
Park H, Quinlan J, Thornton E, Reder LM (2004) The effect of midazolam on visual search: implications for understanding amnesia. Proc Natl Acad Sci USA 101(51):17879–17883
Peters J, Daum I, Gizewski E, Forsting M, Suchan B (2009) Associations evoked during memory encoding recruit the context-network. Hippocampus 19:141–151
Piekema C, Kessels RP, Mars RB, Petersson KM, Fernandez G (2006) The right hippocampus participates in short-term memory maintenance of object-location associations. Neuroimage 33:374–382
Pohlack ST, Nees F, Ruttorf M, Witt SH, Nieratschker V, Rietschel M, Flor H (2011) Risk variant for schizophrenia in the neurogranin gene impacts on hippocampus activation during contextual fear conditioning. Mol Psychiatry 16(11):1072–1073
Pohlack ST, Nees F, Liebscher C, Cacciaglia R, Diener SJ, Ridder S et al (2012) Hippocampal but not amygdalar volume affects contextual fear conditioning in humans. Hum Brain Mapp 33(2):478–488
Pohlack ST, Meyer P, Cacciaglia R, Liebscher C, Ridder S, Flor H (2014) Bigger is better! Hippocampal volume and declarative memory performance in healthy young men. Brain Struct Funct 219(1):255–267
Preston AR, Gabrieli JD (2008) Dissociation between explicit memory and configural memory in the human medial temporal lobe. Cereb Cortex 18:2192–2207
Rajah MN, Kromas M, Han JE, Pruessner JC (2010) Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults. Neuropsychologia 48:4020–4030
Ranganath C (2010) A unified framework for the functional organization of the medial temporal lobes and the phenomenology of episodic memory. Hippocampus 20(11):1263–1290
Reder LM, Park H, Kieffaber PD (2009) Memory systems do not divide on consciousness: reinterpreting memory in terms of activation and binding. Psychol Bull 135:23–49
Rosen ML, Stern CE, Devaney KJ, Somers DC (2017) Cortical and subcortical contributions to long-term memory-guided visuospatial attention. Cereb Cortex 27:1–13
Rudy JW, Huff NC, Matus-Amat P (2004) Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev 28(7):675–685
Ryan JD, Cohen NJ (2003) Evaluating the neuropsychological dissociation evidence for multiple memory systems. Cogn Affect Behav Neurosci 3:168–185
Squire LR (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177
Staresina BP, Davachi L (2008) Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J Cogn Neurosci 20:1478–1489
Tulving E, Schacter DL (1990) Priming and human memory systems. Science 247:301–306
Turk-Browne NB, Scholl BJ, Chun MM, Johnson MK (2008) Neural evidence of statistical learning: efficient detection of visual regularities without awareness. J Cogn Neurosci 21:1934–1945
Turk-Browne NB, Scholl BJ, Johnson MK, Chun MM (2010) Implicit perceptual anticipation triggered by statistical learning. J Neurosci 30:11177–11187
Turk-Browne NB, Golomb JD, Chun MM (2013) Complementary attentional components of successful memory encoding. Neuroimage 66:553–562
Westerberg CE, Miller BB, Reber PJ, Cohen NJ, Paller KA (2011) Neural correlates of contextual cueing are modulated by explicit learning. Neuropsychologia 49:3439–3447
Winkelmann T, Thayer JF, Pohlack S, Nees F, Grimm O, Flor H (2017) Structural brain correlates of heart rate variability in a healthy young adult population. Brain Struct Funct 222(2):1061–1068
Wittchen HU, Wunderlich U, Gruschwitz S, Zaudig M (1997): SKID-I. Strukturiertes Klinisches Interview für DSM-IV. “Structured Clinical Interview for DSM-IV”. Hogrefe, Gottingen
Acknowledgements
This research was supported by Grant SFB636⁄C1 from the Deutsche Forschungsgemeinschaft to HF and, Administrative Department of Science, Technology and Innovation (Colciencias) Grant to MR.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
The authors state that this manuscript is in accordance with the Authorship statement of ethical standards for manuscripts submitted to Brain Structure and Function.
Ethical approval
The Ethics Committee of the Medical Faculty Mannheim of the University of Heidelberg approved the study.
Informed consent
We obtained written informed consent from all persons before participation.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Frauke Nees and Herta Flor joint last authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table
1. Summary of linear regression analysis results predicting contextual cueing performance from cortical volumes of Desikan parcellations, including only those participants who showed a positive contextual cueing effect. (PNG 1939 kb)
Rights and permissions
About this article
Cite this article
Rosero, M.A., Winkelmann, T., Pohlack, S. et al. Memory-guided attention: bilateral hippocampal volume positively predicts implicit contextual learning. Brain Struct Funct 224, 1999–2008 (2019). https://doi.org/10.1007/s00429-019-01887-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-019-01887-9