Unconscious relational encoding depends on hippocampus

Brain

Volumn 137, Issue 12, 2014, Pages 3355-3370

  Duss, Simone B ^a   Reber, Thomas P ^a   Hänggi, Jürgen ^b   Schwab, Simon ^a,c   Wiest, Roland ^c   Müri, René M ^a,c   Brugger, Peter ^d   Gutbrod, Klemens ^a,c   Henke, Katharina ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Flexible; Implicit; Nondeclarative; Relational; Subliminal

Indexed keywords

ADULT; AMNESIA; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; BRAIN SIZE; CINGULATE GYRUS; CLINICAL ARTICLE; CONSCIOUSNESS; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; GLOBUS PALLIDUS; GRAY MATTER; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; LANGUAGE; LEFT HEMISPHERE; LINGUAL GYRUS; MALE; MEMORY; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; NEOCORTEX; NEUROIMAGING; NEUROLOGIC EXAMINATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE SCANNER; PARAHIPPOCAMPAL GYRUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; RESTING STATE NETWORK; SEMANTICS; SINGLE ITEM TASK; SUPERIOR FRONTAL GYRUS; SUPERIOR TEMPORAL GYRUS; THALAMUS; UNCONSCIOUS RELATIONAL ENCODING; UNCUS; VOLUMETRY; VOXEL BASED MORPHOMETRY; IMAGE PROCESSING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; AMNESIA; CONSCIOUSNESS; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MEMORY; MIDDLE AGED; NEUROIMAGING; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84922376496     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu270     Document Type: Article

References (52)

1. Bar M, Tootell RB, Schacter DL, Greve DN, Fischl B, Mendola JD, et al. Cortical mechanisms specific to explicit visual object recognition. Neuron 2001; 29: 529-35.
2. Binder JR, Desai RH, Graves WW, Conant LL. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroi-maging studies. Cereb Cortex 2009; 19: 2767-96.
3. Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, et al. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 2004; 23: 724-38.
4. Caulo M, Van Hecke J, Toma L, Ferretti A, Tartaro A, Colosimo C, et al. Functional MRI study of diencephalic amnesia in Wernicke-Korsakoff syndrome. Brain 2005; 128: 1584-94.
5. Chen J, Olsen RK, Preston AR, Glover GH, Wagner AD. Associative retrieval processes in the human medial temporal lobe: Hippocampal retrieval success and CA1 mismatch detection. Learn Mem 2011; 18: 523-8.
6. Cohen NJ, Eichenbaum H. Memory, amnesia and the hippocampal system. Cambridge: MIT Press; 1993.
7. Degonda N, Mondadori CR, Bosshardt S, Schmidt CF, Boesiger P, Nitsch RM, et al. Implicit associative learning engages the hippocampus and interacts with explicit associative learning. Neuron 2005; 46: 505-20.
8. Duncan K, Ketz N, Inati SJ, Davachi L. Evidence for area CA1 as a match/mismatch detector: a high-resolution fMRI study of the human hippocampus. Hippocampus 2012; 22: 389-98.
9. Duss SB, Oggier S, Reber TP, Henke K. Formation of semantic associations between subliminally presented face-word pairs. Conscious Cogn 2011; 20: 928-35.
10. Free SL, Bergin PS, Fish DR, Cook MJ, Shorvon SD, Stevens JM. Methods for normalization of hippocampal volumes measured with MR. Am J Neuroradiol 1995; 16: 637-43.
11. Giovanello KS, Verfaellie M, Keane MM. Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 2003; 3: 186-94.
12. Greenwald AG, Klinger MR, Schuh ES. Activation by marginally perceptible ("subliminal") stimuli: dissociation of unconscious from conscious cognition. J Exp Psychol Gen 1995; 124: 22-42.
13. Henke K. A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 2010; 11: 523-32.
14. Henke K, Treyer V, Nagy ET, Kneifel S, Dürsteler M, Nitsch RM, et al. Active hippocampus during nonconscious memories. Conscious Cogn 2003a; 12: 31-48.
15. Henke K, Mondadori CR, Treyer V, Nitsch RM, Buck A, Hock C. Nonconscious formation and reactivation of semantic associations by way of the medial temporal lobe. Neuropsychologia 2003b; 41: 863-76.
16. Henke K, Reber TP, Duss SB. Integrating events across levels of consciousness. Front Behav Neurosci 2013; 7: 68.
17. Henson RNA. Neuroimaging studies of priming. Prog Neurobiol 2003; 70: 53-81.
18. Kan IP, Alexander MP, Verfaellie M. Contribution of prior semantic knowledge to new episodic learning in amnesia. J Cogn Neurosci 2009; 21: 938-44.
19. Kan IP, Giovanello KS, Schnyer DM, Makris N, Verfaellie M. Role of the medial temporal lobes in relational memory: neuropsychological evidence from a cued recognition paradigm. Neuropsychologia 2007; 45: 2589-97.
20. Kleinknecht KR, Bedenk BT, Kaltwasser SF, Grunecker B, Yen YC, Czisch M, et al. Hippocampus-dependent place learning enables spatial flexibility in C57BL6/N mice. Front Behav Neurosci 2012; 6: 87.
21. Konrad C, Ukas T, Nebel C, Arolt V, Toga AW, Narr KL. Defining the human hippocampus in cerebral magnetic resonance images-an overview of current segmentation protocols. Neuroimage 2009; 47: 1185-95.
22. Krawczyk DC. The cognition and neuroscience of relational reasoning. Brain Res 2012; 1428: 13-23.
23. Kovács G, Vogels R, Orban GA. Cortical correlate of pattern backward masking. Proc Natl Acad Sci USA 1995; 92: 5587-91.
24. Kumaran D, Maguire EA. Match-mismatch processes underlie human hippocampal responses to associative novelty. J Neurosci 2007; 27: 8517-24.
25. Li YO, Adali T, Calhoun VD. Estimating the number of independent components for functional magnetic resonance imaging data. Hum Brain Mapp 2007; 28: 1251-66.
26. Maguire EA, Frith CD, Rudge P, Cipolotti L. The effect of adult-acquired hippocampal damage on memory retrieval: an fMRI study. Neuroimage 2005; 27: 146-52.
27. Maguire EA, Vargha-Khadem F, Mishkin M. The effects of bilateral hip-pocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 2001; 124: 1156-70.
28. Mayes AR, Holdstock JS, Isaac CL, Hunkin NM, Roberts N. Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 2002; 12: 325-40.
29. McKone E, Slee JA. Explicit contamination in "implicit" memory for new associations. Mem Cognit 1997; 25: 352-66.
30. 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.
31. Moutoussis K, Zeki S. The relationship between cortical activation and perception investigated with invisible stimuli. Proc Natl Acad Sci USA 2002; 99: 9527-32.
32. O'Reilly RC, Rudy JW. Computational principles of learning in the neo-cortex and hippocampus. Hippocampus 2000; 10: 389-97.
33. Patterson K, Nestor PJ, Rogers TT. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 2007; 8: 976-87.
34. Reber TP, Henke K. Rapid formation and flexible expression of memories of subliminal word pairs. Front Psychol 2011; 2: 343.
35. Reber TP, Henke K. Integrating unseen events over time. Conscious Cogn 2012; 21: 953-60.
36. Reber TP, Luechinger R, Boesiger P, Henke K. Unconscious relational inference recruits the hippocampus. J Neurosci 2012; 32: 6138-48.
37. Reber TP, Luechinger R, Boesiger P, Henke K. Detecting analogies unconsciously. Front Behav Neurosci 2014; 8: 9.
38. Ridgway GR, Omar R, Ourselin S, Hill DL, Warren JD, Fox NC. Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage 2009; 44: 99-111.
39. Rolls ET, Tovee MJ. Processing speed in the cerebral cortex and the neurophysiology of visual masking. Proc Biol Sci 1994; 257: 9-15.
40. Rolls ET, Tovee MJ, Panzeri S. The neurophysiology of backward visual masking: information analysis. J Cogn Neurosci 1999; 11: 300-11.
41. Schacter DL. Memory and awareness. Science 1998; 280: 59-60.
42. Schacter DL, Graf P. Preserved learning in amnesic patients-perspectives from research on direct priming. J Clin Exp Neuropsychol 1986; 8: 727-43.
43. Segaert K, Weber K, de Lange FP, Petersson KM, Hagoort P. The suppression of repetition enhancement: a review of fMRI studies. Neuropsychologia 2013; 51: 59-66.
44. Shimamura AP, Squire LR. Impaired priming of new associations in amnesia. J Exp Psychol Learn Mem Cogn 1989; 15: 721-8.
45. Smith CN, Squire LR. Experience-dependent eye movements reflect hippocampus-dependent (aware) memory. J Neurosci 2008; 28: 12825-33.
46. Squire LR, Zola SM. Structure and function of declarative and nonde-clarative memory systems. Proc Natl Acad Sci USA 1996; 93: 13515-22.
47. Srinivasan R, Russell DP, Edelman GM, Tononi G. Increased synchronization of neuromagnetic responses during conscious perception. J Neurosci 1999; 19: 5435-48.
48. Tulving E. How many memory-systems are there. Am Psychol 1985; 40: 385-98.
49. Tulving E. Episodic memory: From mind to brain. Annu Rev Psychol 2002; 53: 1-25.
50. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273-89.
51. van Kesteren MTR, Ruiter DJ, Fernández G, Henson RN. How schema and novelty augment memory formation. Trends Neurosci 2012; 35: 211-9.
52. Verfaelllie M, LaRocque KF, Keane MM. Intact implicit verbal relational memory in medial temporal lobe amnesia. Neuropsychologia 2012; 50: 2100-6.