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PLOS Biology  2006 

An Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus

DOI: 10.1371/journal.pbio.0040424

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Abstract:

The ability to identify and react to novelty within the environment is fundamental to survival. Computational models emphasize the potential role of the hippocampus in novelty detection, its unique anatomical circuitry making it ideally suited to act as a comparator between past and present experience. The hippocampus, therefore, is viewed to detect associative mismatches between what is expected based on retrieval of past experience and current sensory input. However, direct evidence that the human hippocampus performs such operations is lacking. We explored brain responses to novel sequences of objects using functional magnetic resonance imaging (fMRI), while subjects performed an incidental target detection task. Our results demonstrate that hippocampal activation was maximal when prior predictions concerning which object would appear next in a sequence were violated by sensory reality. In so doing, we establish the biological reality of associative match-mismatch computations within the human hippocampus, a process widely held to play a cardinal role in novelty detection. Our results also suggest that the hippocampus may generate predictions about how future events will unfold, and critically detect when these expectancies are violated, even when task demands do not require it. The present study also offers broader insights into the nature of essential computations carried out by the hippocampus, which may also underpin its unique contribution to episodic memory.

References

[1]  Brown MW, Aggleton JP (2001) Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51–61.
[2]  Ranganath C, Rainer G (2003) Neural mechanisms for detecting and remembering novel events. Nat Rev Neurosci 4: 193–202.
[3]  Hasselmo ME, Wyble BP, Wallenstein GV (1996) Encoding and retrieval of episodic memories: Role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6: 693–708.
[4]  Vinogradova OS (2001) Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11: 578–598.
[5]  Lisman JE, Otmakhova NA (2001) Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11: 551–568.
[6]  Knight R (1996) Contribution of human hippocampal region to novelty detection. Nature 383: 256–259.
[7]  Otto T, Eichenbaum H (1992) Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: evidence for hippocampal processing in recognition memory. Hippocampus 2: 323–334.
[8]  Gray JA (1982) The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Oxford: Oxford University Press. 548 p.
[9]  Sokolov EN (1963) Higher nervous functions: The orienting reflex. Annu Rev Physiol 25: 545–580.
[10]  Lisman JE (1999) Relating hippocampal circuitry to function: Recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22: 233–242.
[11]  Lisman JE, Grace AA (2005) The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron 46: 703–713.
[12]  O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford: Oxford University Press. 570 p.
[13]  Fyhn M, Molden S, Hollup S, Moser MB, Moser E (2002) Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35: 555–566.
[14]  Honey RC, Watt A, Good M (1998) Hippocampal lesions disrupt an associative mismatch process. J Neurosci 18: 2226–2230.
[15]  O'Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51: 78–109.
[16]  Duzel E, Habib R, Rotte M, Guderian S, Tulving E, et al. (2003) Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus configurations. J Neurosci 23: 9439–9444.
[17]  Kohler S, Danckert S, Gati JS, Menon RS (2005) Novelty responses to relational and non-relational information in the hippocampus and the parahippocampal region: A comparison based on event-related fMRI. Hippocampus 15: 763–774.
[18]  Tulving E, Markowitsch HJ, Craik FE, Habib R, Houle S (1996) Novelty and familiarity activations in PET studies of memory encoding and retrieval. Cereb Cortex 6: 71–79.
[19]  Tulving E, Markowitsch HJ, Kapur S, Habib R, Houle S (1994) Novelty encoding networks in the human brain: Positron emission tomography data. Neuroreport 5: 2525–2528.
[20]  Stern CE, Corkin S, Gonzalez RG, Guimaraes AR, Baker JR, et al. (1996) The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. Proc Natl Acad Sci U S A 93: 8660–8665.
[21]  Martin A, Wiggs CL, Weisberg J (1997) Modulation of human medial temporal lobe activity by form, meaning, and experience. Hippocampus 7: 587–593.
[22]  Rutishauser U, Mamelak AN, Schuman EM (2006) Single-trial learning of novel stimuli by individual neurons of the human hippocampus-amygdala complex. Neuron 49: 805–813.
[23]  Meeter M, Murre JM, Talamini LM (2004) Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits. Hippocampus 14: 722–741.
[24]  Lee I, Hunsaker MR, Kesner RP (2005) The role of hippocampal subregions in detecting spatial novelty. Behav Neurosci 119: 145–153.
[25]  Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21: 317–323.
[26]  Rawlins JN (1985) Associations across time: The hippocampus as a temporary memory store. Behav Brain Sci 8: 479–528.
[27]  Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5: 458–462.
[28]  Morris RG, Frey U (1997) Hippocampal synaptic plasticity: Role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B Biol Sci 352: 1489–1503.
[29]  Eichenbaum H (2004) Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109–120.
[30]  Levy WB (1996) A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6: 579–590.
[31]  Yamaguchi S, Hale LA, D'Esposito M, Knight RT (2004) Rapid prefrontal-hippocampal habituation to novel events. J Neurosci 24: 5356–5363.
[32]  Henson RN (1998) Short-term memory for serial order: The Start-End Model. Cognit Psychol 36: 73–137.
[33]  Hitch GJ, Fastame MC, Flude B (2005) How is the serial order of a verbal sequence coded? Some comparisons between models. Memory 13: 247–258.
[34]  Burgess N, Hitch G (2005) Computational models of working memory: Putting long-term memory into context. Trends Cogn Sci 9: 535–541.
[35]  Rose M, Haider H, Buchel C (2005) Unconscious detection of implicit expectancies. J Cogn Neurosci 17: 918–927.
[36]  Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: Neural models of stimulus-specific effects. Trends Cogn Sci 10: 14–23.
[37]  Henson RN, Cansino S, Herron JE, Robb WG, Rugg MD (2003) A familiarity signal in human anterior medial temporal cortex? Hippocampus 13: 301–304.
[38]  Erickson CA, Desimone R (1999) Responses of macaque perirhinal neurons during and after visual stimulus association learning. J Neurosci 19: 10404–10416.
[39]  Wirth S, Yanike M, Frank LM, Smith AC, Brown EN, et al. (2003) Single neurons in the monkey hippocampus and learning of new associations. Science 300: 1578–1581.
[40]  Messinger A, Squire LR, Zola SM, Albright TD (2001) Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc Natl Acad Sci U S A 98: 12239–12244.
[41]  Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27: 279–306.
[42]  Kirwan CB, Stark CE (2004) Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus 14: 919–930.
[43]  Marr D (1971) Simple memory: A theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262: 23–81.
[44]  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.
[45]  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.
[46]  Ranganath C, Blumenfeld RS (2005) Doubts about double dissociations between short- and long-term memory. Trends Cogn Sci 9: 374–380.
[47]  Suzuki WA (1999) The long and the short of it: Memory signals in the medial temporal lobe. Neuron 24: 295–298.
[48]  Buffalo EA, Reber PJ, Squire LR (1998) The human perirhinal cortex and recognition memory. Hippocampus 8: 330–339.
[49]  Nichols EA, Kao YC, Verfaellie M, Gabrieli JD (2006) Working memory and long-term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus 16: 604–616.
[50]  Olson IR, Page K, Moore KS, Chatterjee A, Verfaellie M (2006) Working memory for conjunctions relies on the medial temporal lobe. J Neurosci 26: 4596–4601.
[51]  Stern CE, Sherman SJ, Kirchhoff BA, Hasselmo ME (2001) Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli. Hippocampus 11: 337–346.
[52]  Schultz W (2006) Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 57: 87–115.
[53]  Corlett PR, Aitken MR, Dickinson A, Shanks DR, Honey GD, et al. (2004) Prediction error during retrospective revaluation of causal associations in humans: fMRI evidence in favor of an associative model of learning. Neuron 44: 877–888.
[54]  Seymour B, O'Doherty JP, Dayan P, Koltzenburg M, Jones AK, et al. (2004) Temporal difference models describe higher-order learning in humans. Nature 429: 664–667.
[55]  Moser EI, Moser MB (2003) One-shot memory in hippocampal CA3 networks. Neuron 38: 147–148.
[56]  Soltani M, Knight RT (2000) Neural origins of the P300. Crit Rev Neurobiol 14: 199–224.
[57]  Strange BA, Dolan RJ (2001) Adaptive anterior hippocampal responses to oddball stimuli. Hippocampus 11: 690–698.
[58]  Strange BA, Duggins A, Penny W, Dolan RJ, Friston KJ (2005) Information theory, novelty and hippocampal responses: Unpredicted or unpredictable? Neural Netw 18: 225–230.
[59]  Harrison LM, Duggins A, Friston KJ (2006) Encoding uncertainty in the hippocampus. Neural Netw 19: 535–546.
[60]  Alain C, Woods DL, Knight RT (1998) A distributed cortical network for auditory sensory memory in humans. Brain Res 812: 23–37.
[61]  Frackowiak RS, Friston KJ, Frith CD, Dolan RJ, Price CJ, et al. (2004) Human brain function. New York: Elsevier Academic Press. 1144 p.
[62]  Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, et al. (1998) Event-related fMRI: Characterizing differential responses. Neuroimage 7: 30–40.
[63]  Friston KJ, Zarahn E, Josephs O, Henson RN, Dale AM (1999) Stochastic designs in event-related fMRI. Neuroimage 10: 607–619.
[64]  Deichmann R, Gottfried JA, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19: 430–441.
[65]  Weiskopf N, Hutton C, Josephs O, Deichmann R (2005) Optimal EPI parameters for BOLD sensitivity dropout reduction: A whole brain map. #1543. Proceedings of the 13th International Society for Magnetic Resonance in Medicine (ISMRM).

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