Episodic memory; Functional neuroimaging; Scene construction; Self-generated thought; Visuo-spatial processing
Abstract :
[en] Episodic memories are typically composed of perceptual information derived from the external
environment and representations of internal states (e.g., one’s thoughts during prior episodes). To date, however, research has mostly focused on the remembrance of external stimuli, such that little is known about how internal mentation is represented within episodic memory. In the present fMRI study, we examined the neural correlates of these two components of episodic memories using a novel method of cuing memories from photographs taken during real-life events. We found that, compared to corresponding semantic memory tasks, memories for internal thoughts and external elements were associated with activity in brain areas supporting episodic recollection. Most importantly, however, the two kinds of memories also showed differential activation in large-scale brain networks: the remembrance of external elements was
associated with greater activity in the dorsal attention network, whereas memories of internal thoughts mainly recruited default network areas. These findings shed new light on the representation of internal and external aspects of prior experience within episodic memory. The default network may contribute to the reinstatement of thoughts experienced during past events, whereas the dorsal attention network may support the allocation of attention to visuo-spatial features within episodic memory representations.
Addis DR, Knapp K, Roberts RP, Schacter DL. 2012. Routes to the past: neural substrates of direct and generative autobiographical memory retrieval. Neuroimage. 59:2908-2922.
Addis DR, McIntosh AR, Moscovitch M, Crawley AP, McAndrews MP. 2004. Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach. Neuroimage. 23:1460-1471.
Andersson JL, Hutton C, Ashburner J, Turner R, Friston K. 2001. Modeling geometric deformations in EPI time series. Neuroimage. 13:903-919.
Andrews-Hanna JR. 2012. The brain's default network and its adaptive role in internal mentation. Neuroscientist. 18:251-270.
Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL. 2010. Functional-anatomic fractionation of the brain's default network. Neuron. 65:550-562.
Andrews-Hanna JR, Saxe R, Yarkoni T. 2014. Contributions of episodic retrieval and mentalizing to autobiographical thought: evidence from functional neuroimaging, restingstate connectivity, and fMRI meta-analyses. Neuroimage. 91:324-335.
Andrews-Hanna JR, Smallwood J, Spreng RN. 2014. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann NY Acad Sci. 1316:29-52.
Baddeley A, Aggleton JP, Conway MA. 2002. Episodic memory: new directions in research. New York: Oxford University Press.
Bar M. 2004. Visual objects in context. Nat Rev Neurosci. 5:617-629.
Beaty RE, Benedek M, Silvia PJ, Schacter DL. 2016. Creative cognition and brain network dynamics. Trends Cogn Sci. 20:87-95.
Benoit RG, Schacter DL. 2015. Specifying the core network supporting episodic simulation and episodic memory by activation likelihood estimation. Neuropsychologia. 75:450-457.
Binder JR, Desai RH, Graves WW, Conant LL. 2009. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex. 19:2767-2796.
Bonnici HM, Chadwick MJ, Maguire EA. 2013. Representations of recent and remote autobiographical memories in hippocampal subfields. Hippocampus. 23:849-854.
Bonnici HM, Maguire EA. 2017. Two years later-revisiting autobiographical memory representations in vmPFC and hippocampus. Neuropsychologia.
Brewer WF. 1988. Memory for randomly sampled autobiographical events. In: Neisser U, Winograd E, editors. Remembering reconsidered: ecological and traditional approaches to the study of memory. Cambridge, UK: Cambridge University Press. p. 21-90.
Cabeza R, Ciaramelli E, Olson IR, Moscovitch M. 2008. The parietal cortex and episodic memory: an attentional account. Nat Rev Neurosci. 9:613-625.
Cabeza R, St Jacques P. 2007. Functional neuroimaging of autobiographical memory. Trends Cogn Sci. 11:219-227.
Chen H-Y, Gilmore AW, Nelson SM, McDermott KB. 2017. Are there multiple kinds of episodic memory? An fMRI investigation comparing autobiographical and recognition memory tasks. J Neurosci. 37:2764-2775.
Chow TE, Rissman J. 2017. Neurocognitive mechanisms of realworld autobiographical memory retrieval: insights from studies using wearable camera technology. Ann NY Acad Sci. 1396:202-221.
Christoff K, Irving ZC, Fox KC, Spreng RN, Andrews-Hanna JR. 2016. Mind-wandering as spontaneous thought: a dynamic framework. Nat Rev Neurosci. 17:718-731.
Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 3:201-215.
Crittenden BM, Mitchell DJ, Duncan J. 2015. Recruitment of the default mode network during a demanding act of executive control. eLife. 4:e06481.
D'Argembeau A. 2013. On the role of the ventromedial prefrontal cortex in self-processing: the valuation hypothesis. Front Hum Neurosci. 7:372.
Danker JF, Anderson JR. 2010. The ghosts of brain states past: remembering reactivates the brain regions engaged during encoding. Psychol Bull. 136:87-102.
Desrochers A, Thompson GL. 2009. Subjective frequency and imageability ratings for 3, 600 French nouns. Behav Res Methods. 41:546-557.
Dixon ML, Andrews-Hanna JR, Spreng RN, Irving ZC, Mills C, Girn M, Christoff K. 2017. Interactions between the default network and dorsal attention network vary across default subsystems, time, and cognitive states. NeuroImage. 147:632-649.
Dobbins IG, Wagner AD. 2005. Domain-general and domainsensitive prefrontal mechanisms for recollecting events and detecting novelty. Cereb Cortex. 15:1768-1778.
Ellamil M, Dobson C, Beeman M, Christoff K. 2012. Evaluative and generative modes of thought during the creative process. Neuroimage. 59:1783-1794.
Ford JH, Kensinger EA. 2016. Effects of internal and external vividness on hippocampal connectivity during memory retrieval. Neurobiol Learn Mem. 134 Pt A:78-90.
Fox KC, Spreng RN, Ellamil M, Andrews-Hanna JR, Christoff K. 2015. The wandering brain: meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes. Neuroimage. 111:611-621.
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. 2005. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA. 102:9673-9678.
Ganis G, Thompson WL, Kosslyn SM. 2004. Brain areas underlying visual mental imagery and visual perception: an fMRI study. Cogn Brain Res. 20:226-241.
Gao W, Lin W. 2012. Frontal parietal control network regulates the anti-correlated default and dorsal attention networks. Hum Brain Mapp. 33:192-202.
Gilboa A, Marlatte H. 2017. Neurobiology of schemas and schema-mediated memory. Trends Cogn Sci. 21:618-631.
Gilmore AW, Nelson SM, Chen H-Y, McDermott KB. 2017. Taskrelated and resting-state fMRI identify distinct networks that preferentially support remembering the past and imagining the future. Neuropsychologia.
Gordon AM, Rissman J, Kiani R, Wagner AD. 2014. Cortical reinstatement mediates the relationship between contentspecific encoding activity and subsequent recollection decisions. Cereb Cortex. 24:3350-3364.
Hashtroudi S, Johnson MK, Chrosniak LD. 1990. Aging and qualitative characteristics of memories for perceived and imagined complex events. Psychol Aging. 5:119-126.
Horton CL, Conway MA, Cohen G. 2007. Memory for thoughts and dreams. In: Cohen G, Conway MA, editors. Memory in the real world. New York: Psychology Press. p. 269-303.
Hutton C, Bork A, Josephs O, Deichmann R, Ashburner J, Turner R. 2002. Image distortion correction in fMRI: a quantitative evaluation. Neuroimage. 16:217-240.
Johnson MK. 1988a. Reality monitoring: an experimental phenomenological approach. J Exp Psychol Gen. 117:390-394.
Johnson MK, Foley MA, Suengas AG, Raye CL. 1988b. Phenomenal characteristics of memories for perceived and imagined autobiographical events. J Exp Psychol Gen. 117:371-376.
Kelley W, Macrae C, Wyland C, Caglar S, Inati S, Heatherton T. 2002. Finding the self?: An event-related fMRI study. J Cogn Neurosci. 14:785-794.
Kim H. 2012. A dual-subsystem model of the brain's default network: self-referential processing, memory retrieval processes, and autobiographical memory retrieval. Neuroimage. 61:966-977.
Kim H. 2016. Default network activation during episodic and semantic memory retrieval: a selective meta-analytic comparison. Neuropsychologia. 80:35-46.
Konishi M, McLaren DG, Engen H, Smallwood J. 2015. Shaped by the past: the default mode network supports cognition that is independent of immediate perceptual input. PLoS One. 10: e0132209.
Kragel JE, Polyn SM. 2015. Functional interactions between largescale networks during memory search. Cereb Cortex. 25:667-679.
Lin W-J, Horner AJ, Burgess N. 2016. Ventromedial prefrontal cortex, adding value to autobiographical memories. Sci Rep. 6:28630.
Maillet D, Rajah MN. 2014. Age-related differences in brain activity in the subsequent memory paradigm: a metaanalysis. Neurosci Biobehav Rev. 45:246-257.
Martinelli P, Sperduti M, Piolino P. 2013. Neural substrates of the self-memory system: new insights from a metaanalysis. Hum Brain Mapp. 34:1515-1529.
McDermott KB, Szpunar KK, Christ SE. 2009. Laboratory-based and autobiographical retrieval tasks differ substantially in their neural substrates. Neuropsychologia. 47:2290-2298.
Moscovitch M, Cabeza R, Winocur G, Nadel L. 2016. Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol. 67:105-134.
Muhlert N, Milton F, Butler CR, Kapur N, Zeman AZ. 2010. Accelerated forgetting of real-life events in Transient Epileptic Amnesia. Neuropsychologia. 48:3235-3244.
Murray RJ, Schaer M, Debbané M. 2012. Degrees of separation: a quantitative neuroimaging meta-analysis investigating selfspecificity and shared neural activation between self- and other-reflection. Neurosci Biobehav Rev. 36:1043-1059.
Nobre AC, Coull JT, Maquet P, Frith CD, Vandenberghe R, Mesulam MM. 2004. Orienting attention to locations in perceptual versus mental representations. J Cogn Neurosci. 16:363-373.
Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H, Panksepp J. 2006. Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage. 31:440-457.
Pearson J, Naselaris T, Holmes EA, Kosslyn SM. 2015. Mental imagery: functional mechanisms and clinical applications. Trends Cogn Sci. 19:590-602.
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. 2001. A default mode of brain function. Proc Natl Acad Sci USA. 98:676-682.
Renoult L, Davidson PS, Palombo DJ, Moscovitch M, Levine B. 2012. Personal semantics: at the crossroads of semantic and episodic memory. Trends Cogn Sci. 16:550-558.
Schacter DL, Addis DR, Hassabis D, Martin VC, Spreng RN, Szpunar KK. 2012. The future of memory: remembering, imagining, and the brain. Neuron. 76:677-694.
Schacter DL, Benoit RG, De Brigard F, Szpunar KK. 2015. Episodic future thinking and episodic counterfactual thinking: intersections between memory and decisions. Neurobiol Learn Mem. 117:14-21.
Sestieri C, Shulman GL, Corbetta M. 2010. Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex. J Neurosci. 30:8445-8456.
Sestieri C, Shulman GL, Corbetta M. 2017. The contribution of the human posterior parietal cortex to episodic memory. Nat Rev Neurosci. 18:183-192.
Simons JS, Garrison JR, Johnson MK. 2017. Brain mechanisms of reality monitoring. Trends Cogn Sci. 21:462-473.
Simons JS, Owen AM, Fletcher PC, Burgess PW. 2005. Anterior prefrontal cortex and the recollection of contextual information. Neuropsychologia. 43:1774-1783.
Smallwood J, Schooler JW. 2015. The science of mind wandering: empirically navigating the stream of consciousness. Annu Rev Psychol. 66:487-518.
Spreng RN, Mar RA, Kim AS. 2009. The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative metaanalysis. J Cogn Neurosci. 21:489-510.
Spreng RN, Sepulcre J, Turner GR, Stevens WD, Schacter DL. 2013. Intrinsic architecture underlying the relations among the default, dorsal attention, and frontoparietal control networks of the human brain. J Cogn Neurosci. 25:74-86.
Spreng RN, Stevens WD, Chamberlain JP, Gilmore AW, Schacter DL. 2010. Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage. 53:303-317.
St Jacques PL, Cabeza R. 2012. Neural basis of autobiographical memory. In: Ghetti S, Bauer PJ, editors. Origins and development of recollection. New York: Oxford University Press. p. 188-218.
St Jacques PL, De Brigard F. 2015. Neural correlates of autobiographical memory: methodological considerations. In: Addis DR, Barense M, Duarte A, editors. TheWiley handbook on the cognitive neuroscience of memory. New York, NY: Wiley-Blackwell. p. 265-286.
St Jacques PL, Olm C, Schacter DL. 2013. Neural mechanisms of reactivation-induced updating that enhance and distort memory. Proc Natl Acad Sci USA. 110:19671-19678.
Stawarczyk D, D'Argembeau A. 2015. Neural correlates of personal goal processing during episodic future thinking and mind-wandering: an ALE meta-analysis. Hum Brain Mapp. 36:2928-2947.
Stawarczyk D, Majerus S, Maquet P, D'Argembeau A. 2011. Neural correlates of ongoing conscious experience: both task-unrelatedness and stimulus-independence are related to default network activity. PLoS One. 6:e16997.
Szpunar KK. 2010. Episodic future thought: an emerging concept. Perspect Psychol Sci. 5:142-162.
Szpunar KK, Spreng RN, Schacter DL. 2014. A taxonomy of prospection: introducing an organizational framework for future-oriented cognition. Proc Natl Acad Sci USA. 111:18414-18421.
Tulving E. 2002. Episodic memory: from mind to brain. Annu Rev Psychol. 53:1-25.
Turner MS, Simons JS, Gilbert SJ, Frith CD, Burgess PW. 2008. Distinct roles for lateral and medial rostral prefrontal cortex in source monitoring of perceived and imagined events. Neuropsychologia. 46:1442-1453.
van der Meer L, Costafreda S, Aleman A, David AS. 2010. Selfreflection and the brain: a theoretical review and metaanalysis of neuroimaging studies with implications for schizophrenia. Neurosci Biobehav Rev. 34:935-946.
Van Essen DC. 2005. A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. NeuroImage. 28:635-662.
Van Hoeck N, Ma N, Ampe L, Baetens K, Vandekerckhove M, Van Overwalle F. 2013. Counterfactual thinking: an fMRI study on changing the past for a better future. Soc Cogn Affect Neurosci. 8:556-564.
van Kesteren MT, Ruiter DJ, Fernandez G, Henson RN. 2012. How schema and novelty augment memory formation. Trends Neurosci. 35:211-219.
Van Overwalle F. 2009. Social cognition and the brain: a metaanalysis. Hum Brain Mapp. 30:829-858.
Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL. 2008. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol. 100:3328-3342.
Wang J, Baucom LB, Shinkareva SV. 2013. Decoding abstract and concrete concept representations based on single-trial fMRI data. Hum Brain Mapp. 34:1133-1147.
Wang J, Conder JA, Blitzer DN, Shinkareva SV. 2010. Neural representation of abstract and concrete concepts: a metaanalysis of neuroimaging studies. Hum Brain Mapp. 31:1459-1468.
