Hodgetts, CJ

Postans, M

Williams, AN

Williams, Angharad

Postans, Mark

Hodgetts, Carl

Online Research @ Cardiff

Journal ClubEditor’s Note: These short reviews of recent JNeurosci articles, written exclusively by students or postdoctoral fellows, summarizethe important findings of the paper and provide additional insight and commentary. If the authors of the highlighted article havewritten a response to the Journal Club, the response can be found by viewing the Journal Club at www.jneurosci.org. For moreinformation on the format, review process, and purpose of Journal Club articles, please see http://jneurosci.org/content/jneurosci-journal-club.How the Human Brain Segments Continuous ExperienceX Angharad N. Williams, X Mark Postans, and Carl J. HodgettsCardiff University Brain Research Imaging Centre (CUBRIC), School of Psychology, Cardiff University, Cardiff CF10 3AT, United KingdomReview of Ben-Yakov and HensonThe formation and subsequent recall ofcoherent episodes from our past (i.e., ourepisodic memories) relies on the ability toparse the continuous stream of experiencein our daily lives into meaningful chunksor segments (Zacks et al., 2010). This seg-mentation is thought to determine howepisodic memories are organized. Forinstance, elements within an event arebound together more so than individualelements across events (DuBrow and Da-vachi, 2013, 2016), and the ability to seg-ment information is linked to bettersubsequent memory (Sargent et al., 2013).The events we experience and remem-ber are often complex and unfold overtime, but neuroimaging studies of epi-sodic memory have typically used isolatedstatic stimuli. Despite providing tightcontrol over what is seen, and for howlong, there is clearly a disconnect betweenclassic laboratory tests of episodic mem-ory and the construction of event repre-sentations in everyday life. Therefore,researchers have sought to use stimuli thatare more dynamic and naturalistic, suchas discrete film-clips lasting a few seconds.Such studies have found that hippocam-pal activity increases at the immediate off-set of clips and is greater for rememberedversus forgotten episodes (Ben-Yakov andDudai, 2011; Ben-Yakov et al., 2013). Theauthors suggested that this signal mightreflect the laying down of integrated eventmemories. These studies, however, did notexamine how the hippocampus respondsduring continuous experience.To address this question, a recent studyin The Journal of Neuroscience (Ben-Yakovand Henson, 2018) analyzed functionalmagnetic resonance imaging (fMRI) datacollected as participants viewed an 8 minversion of Alfred Hitchcock’s drama“Bang! You’re Dead,” or a longer feature-length version of the film Forrest Gump.To define event segments, or “boundar-ies,” an independent set of participantswas asked to watch the two movies andpress a button whenever they felt an event(“one meaningful unit”) ended and an-other began. These annotations were thenused to examine hippocampal activity atevent boundaries in the two fMRI data-sets. Ben-Yakov and Henson (2018) noteda number of possible perceptual con-founds (e.g., shifts in luminance, colorhistograms, or auditory similarity acrossthe frames of each boundary), but tooksteps to control for these in their analyses.It is important to note that the way moviesare created and edited leads to potentiallydramatic changes in visual and/or audi-tory factors. For example, films are com-posed of a series of scenes with abruptchanges in location, characters, and otherelements. Therefore, although they aremore similar to real life than the static el-ements used in previous experiments,some of the boundaries are unlike thecontinuous transition between events inreal life.Going beyond previous work linkingthe hippocampus to event-boundary pro-cessing (Ben-Yakov and Dudai, 2011;Ben-Yakov et al., 2013; DuBrow and Da-vachi, 2016), Ben-Yakov and Henson(2018) demonstrated that hippocampalactivity increased at the event boundaries,and that activity was greater for boundar-ies for which there was high agreementbetween independent raters. The latter ef-fect remained significant for the longermovie even when controlling for all of theidentified perceptual confounds. The au-thors noted that the shorter movie possi-bly contained too few boundaries relativeto the total number of confounds, thoughthe effect remained for both movies wheneach covariate was added to the modelseparately (Ben-Yakov and Henson, 2018).Notably, Zacks et al. (2010) previouslyfound that perceptual changes (in the phy-sical stimulus, e.g., color/location) were notalways sufficient to establish a neural re-sponse at event boundaries. Some re-sponses, for example, corresponded withmore conceptual changes, involving inter-actions between characters, their goals andintentions, thus underlining the range ofproperties that shape episodic context, overand above perceptual factors (Brunec et al.,2018).Received Dec. 3, 2018; revised Feb. 1, 2019; accepted Feb. 4, 2019.A.N.W. and M.P. are supported by the Medical Research Council (GrantMR/N01233X/1). C.J.H. is supported by a Wellcome Strategic Award(104943/Z/14/Z). We thank Kim Graham, Andrew Lawrence, Rikki Lissa-man, and Samuel Ridgeway for thoughtful discussions.The authors declare no competing financial interests.Correspondence should be addressed to Angharad N. Williams atwilliamsan@cardiff.ac.uk.https://doi.org/10.1523/JNEUROSCI.3041-18.2019Copyright © 2019 Williams et al.This is an open-access article distributed under the terms of theCreative Commons Attribution License Creative Commons Attribution4.0 International, which permits unrestricted use, distribution and reproduc-tion in any medium provided that the original work is properly attributed.3172 • The Journal of Neuroscience, April 24, 2019 • 39(17):3172–3174This finding of Ben-Yakov and Hen-son (2018) dovetails with that of a previ-ous study (Baldassano et al., 2017) thatapplied a computational approach toidentify temporal structure in neuroimag-ing data. Baldassano et al. (2017) foundthat during continuous movie viewing,shifts in cortical activity patterns (includ-ing in angular gyrus, posterior medialcortex, and parahippocampal cortex) co-incided with increased hippocampal ac-tivity. In addition, the cortical activitypatterns matched annotated event bound-aries 35– 40% of the time. Building on this,Ben-Yakov and Henson (2018) sought todirectly test the relationship betweenevent boundaries and hippocampal activ-ity. Here, they used a similar method todetect peaks in hippocampal activityacross time, and subsequently examinedthe alignment between these peaks andevent boundaries. Indeed, a significantcorrespondence was found between thestrongest hippocampal responses and theannotated event boundaries. There were,however, additional peaks in hippocam-pal activity that did not correspond withthe independently defined boundaries.In this context, a potential limitationof this work is that the segmentations weredetermined by an independent sample ofparticipants who did not undergo brainimaging. Critically, the information thatdefines an event boundary, and the gran-ularity at which they are placed, may varyacross individuals according to what feelsnatural to them. Ben-Yakov and Henson(2018) also conducted a binned salienceanalysis (low/medium/high) according tothe number of observers identifying aboundary at a similar point in time. How-ever, despite demonstrating that hip-pocampal activity was modulated by theircoarse “boundary salience” measure, theauthors appropriately concluded thatit could reflect a measure of boundarystrength, coarser levels of event segmenta-tion, or the likelihood of agreement acrossobservers. A question for future work,therefore, is how the brain simultaneouslyprocesses events of varying temporal (andspatial) scales, and how this may differ be-tween individuals (Brunec et al., 2018).Sargent et al. (2013) found that segmenta-tion ability (defined as the degree to whichan individual agreed with the sample) wasrelated to better memory performance(the number of character actions correctlyrecalled after movie viewing). Thus, inter-individual differences in segmentationability may account for individual varia-tion in event memory.Different types of information or typesof boundaries may be represented by dis-tinct hippocampal networks (Ranganathand Ritchey, 2012; Robin and Mosco-vitch, 2017; Murray et al., 2018). For ex-ample, the processing of spatial, temporal,perceptual, and conceptual boundariesmay involve hippocampal interactionswith different cortical and subcortical ar-eas (Brunec et al., 2018). Moreover, thehippocampus itself is a highly heteroge-neous structure, comprising multiple sub-fields (Berron et al., 2017; Hodgetts et al.,2017; Dimsdale-Zucker et al., 2018) andsubdivisions along its anterior–posterioraxis that have distinct connectivity pro-files (Strange et al., 2014; Aggleton et al.,2015). Therefore, different hippocampalsubregions might play distinct but com-plementary roles in event segmentationand memory depending on their connec-tivity with surrounding areas.Subregions of the prefrontal cortex(PFC) may also support different aspectsof event memory (Clewett and Davachi,2017). Specifically, functional connectiv-ity between the hippocampus and medialPFC has been linked to memory integra-tion within an event, whereas activity inboth lateral PFC and the hippocampus atboundaries has been related to the abilityto associate memories across discrete events(DuBrow and Davachi, 2016). Based onthese results, Clewett and Davachi (2017)suggested that hippocampal retrieval mech-anisms, through dynamic interactionswith the PFC, shape the memory integra-tion processes that operate during encod-ing. They proposed that hippocampalretrieval processes may prioritize reacti-vation of the just-encoded informationfor the purpose of integration. Consistentwith this, a related electroencephalogra-phy study demonstrated that the rapidreplay of preceding events, triggered byboundaries, predicted subsequent se-quential recall over those boundaries(Sols et al., 2017).A key unanswered question is whatthese increases in hippocampal activity atevent boundaries represent. As suggestedabove, they may be interpreted as a rapidreplay of the just encountered event tocreate a cohesive representation (Ben-Yakov and Dudai, 2011). Alternatively,this hippocampal signal may reflect (oreven trigger) a rapid shift in situationmodels (mental representations that sum-marize the temporal and contextual de-tails of an event), which in themselves maybe represented within an extended poste-rior hippocampal network (Ranganathand Ritchey, 2012; Baldassano et al., 2017;DuBrow et al., 2017). Further studies in-corporating both event segmentation andmemory will be required to adjudicate be-tween these possible explanations.In summary, Ben-Yakov and Henson(2018) provide compelling evidence forthe role of the hippocampus in segment-ing our continuous experience. They findthat peaks in hippocampal activity areboth sensitive to and specific to subjectiveevent boundaries during naturalistic ex-perience, as assessed using movie viewing.These findings highlight the utility of com-plex, naturalistic stimuli for the study ofhippocampal contributions to event seg-mentation and memory, but they alsoillustrate the unique theoretical and meth-odological challenges that arise as we movetoward more unconstrained, ecologicallyvalid paradigms in cognitive psychologyand fMRI.ReferencesAggleton JP, Wright NF, Rosene DL, Saunders RC(2015) Complementary patterns of directamygdala and hippocampal projections to themacaque prefrontal cortex. Cereb Cortex 25:4351– 4373.Baldassano C, Chen J, Zadbood A, Pillow JW,Hasson U, Norman KA (2017) Discoveringevent structure in continuous narrative per-ception and memory. Neuron 95:709 –721.e5.Ben-Yakov A, Dudai Y (2011) Constructing re-alistic engrams: poststimulus activity ofhippocampus and dorsal striatum predictssubsequent episodic memory. J Neurosci 31:9032–9042.Ben-Yakov A, Henson RN (2018) The hip-pocampal film-editor: sensitivity and spe-cificity to event boundaries in continuousexperience. J Neurosci 38:10057–10068.Ben-Yakov A, Eshel N, Dudai Y (2013) Hip-pocampal immediate poststimulus activity inthe encoding of consecutive naturalistic epi-sodes. J Exp Psychol Gen 142:1255–1263.Berron D, Vieweg P, Hochkeppler A, Pluta JB,Ding SL, Maass A, Luther A, Xie L, Das SR,Wolk DA, Wolbers T, Yushkevich PA, DüzelE, Wisse LEM (2017) A protocol for manualsegmentation of medial temporal lobe subre-gions in 7tesla MRI. Neuroimage 15:466 – 482.Brunec IK, Moscovitch M, Barense MD (2018)Boundaries shape cognitive representations ofspaces and events. Trends Cogn Sci 22:637–650.Clewett D, Davachi L (2017) The ebb and flow ofexperience determines the temporal structureof memory. Curr Opin Behav Sci 17:186 –193.Dimsdale-Zucker HR, Ritchey M, Ekstrom AD,Yonelinas AP, Ranganath C (2018) CA1 andCA3 differentially support spontaneous re-trieval of episodic contexts within human hip-pocampal subfields. Nat Commun 9:294.DuBrow S, Davachi L (2013) The influence ofcontext boundaries on memory for the se-quential order of events. J Exp Psychol Gen142:1277–1286.Williams et al. • Journal Club J. Neurosci., April 24, 2019 • 39(17):3172–3174 • 3173DuBrow S, Davachi L (2016) Temporal bindingwithin and across events. Neurobiol LearnMem 134:107–114.DuBrow S, Rouhani N, Niv Y, Norman KA(2017) Does mental context drift or shift?Curr Opin Behav Sci 17:141–146.Hodgetts CJ, Voets NL, Thomas AG, Clare S, Law-rence AD, Graham KS (2017) Ultra-high-field fMRI reveals a role for the subiculum inscene perceptual discrimination. J Neurosci37:3150 –3159.Murray EA, Wise SP, Graham KS (2018) Repre-sentational specializations of the hippocam-pus in phylogenetic perspective. Neurosci Lett680:4 –12.Ranganath C, Ritchey M (2012) Two corticalsystems for memory-guided behaviour. NatRev Neurosci 13:713–726.Robin J, Moscovitch M (2017) Details, gist and sche-ma: hippocampal–neocortical interactions under-lying recent and remote episodic and spatialmemory. Curr Opin Behav Sci 17:114–123.Sargent JQ, Zacks JM, Hambrick DZ, Zacks RT,Kurby CA, Bailey HR, Eisenberg ML, Beck TM(2013) Event segmentation ability uniquely pre-dicts event memory. Cognition 129:241–255.Sols I, DuBrow S, Davachi L, Fuentemilla L(2017) Event boundaries trigger rapid mem-ory reinstatement of the prior events topromote their representation in long-termmemory. Curr Biol 27:3499 –3504.e4Strange BA, Witter MP, Lein ES, Moser EI (2014)Functional organization of the hippocampallongitudinal axis. Nat Rev Neurosci 15:655–669.Zacks JM, Speer NK, Swallow KM, Maley CJ(2010) The brain’s cutting-room floor: seg-mentation of narrative cinema. Front HumNeurosci 4:168.3174 • J. Neurosci., April 24, 2019 • 39(17):3172–3174 Williams et al. • Journal Club

How the human brain segments continuous experience

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