Encoding of real-life episodic memory commonly involves integration of information as the episode unfolds. Offline processing immediately following event offset is expected to play a role in encoding the episode into memory. In this study, we examined whether distinct human brain activity time-locked to the offset of short narrative audiovisual episodes could predict subsequent memory for the gist of the episodes. We found that a set of brain regions, most prominently the bilateral hippocampus and the bilateral caudate nucleus, exhibit memory-predictive activity time-locked to the stimulus offset. We propose that offline activity in these regions reflects registration to memory of integrated episodes.
AcknowledgementsThis work was supported by the UK Medical Research Council (SUAG/010 RG91365) and a Marie Curie Individual Fellowship (705108) awarded to ABY. The research would not have been possible without the data provided by the Cambridge Centre for Ageing and Neuroscience (Cam-CAN) and the studyforrest project. We thank Michael Hanke for his help with the studyforrest dataset, Christopher Baldassano for support with the cortical pattern shift analysis, and Katherine Storrs for her help with the convoluted neural net analysis. We also thank Roni Tibon, Andrea Greve, Alex Kaula and Alex Quent for valuable feedback. AbstractThe function of the human hippocampus is normally investigated by experimental manipulation of discrete events. Less is unknown about what triggers hippocampal activity during more naturalistic, continuous experience. We hypothesized that the hippocampus would be sensitive to the occurrence of event boundaries, i.e. moments in time identified by observers as a transition between events. To address this, we analysed functional MRI data from two groups: one (N=253, 131 female) who viewed an 8.5min film and another (N=15, 6 female) who viewed a 120min film. We observed a strong hippocampal response at boundaries defined by independent observers, which was modulated by boundary strength (the number of observers that identified each boundary). In the longer film, there were sufficient boundaries to show that this modulation remained after covarying out a large number of perceptual factors. The hippocampus was the only brain region whose response showed a significant monotonic increase with boundary strength in both films, suggesting that modulation by boundary strength is selective to the hippocampus. This hypothesis-driven approach was complemented by a data-driven approach, in which we identified hippocampal-events as moments in time with the strongest hippocampal activity: The correspondence between these hippocampalevents and event boundaries was highly-significant, revealing that the hippocampal response is not only sensitive, but also specific to event boundaries. We conclude that the hippocampus plays an important role in segmenting the continuous experience that is typical of naturalistic settings. Significance statementRecent years have seen the field of human neuroscience research transitioning from experiments with simple stimuli to the study of more complex and naturalistic experience. Nonetheless, our understanding of the function of many brain regions, such as the hippocampus, is based primarily on the study of brief, discrete events. As a result, we know little of what triggers hippocampal activity in real-life settings, when we are exposed to a continuous stream of information. When does the hippocampus "decide" to respond during the encoding of naturalistic experience? We reveal here that hippocampal activity measured by fMRI during film-watching is both sensitive and specific to event boundaries, identifying a potential mechanism whereby event boundaries shape experience by mod...
In the encoding of narrative episodes, the hippocampus exhibits memory-predictive activity time-locked to stimulus offset. In real life, however, events usually occur in succession, raising the question of how the immediate offline processing of one event is affected by presentation of another. To address this issue, participants were presented with brief narrative movie clips in a functional magnetic resonance imaging scanner. Each clip was immediately followed by an additional, unrelated, clip; by a visually scrambled clip with background auditory noises; or by a fixation cross. Memory for the gist of the clips was tested outside the scanner in a cued-recall test 20 min after termination of the study session. The hippocampus responded at the offset of each clip, even when a second clip was presented in immediate succession, suggesting that the hippocampus processes each brief clip as a discrete event. Presentation of a second narrative clip, and to a lesser degree of a scrambled clip, retroactively interfered with memory for the first clip. In parallel, the offline response of the posterior hippocampus to the first movie was reduced. In the anterior hippocampus, presentation of a second clip did not reduce the overall offline response but significantly reduced the difference in activity between remembered and forgotten clips. These findings are in line with the proposition that immediate offline hippocampal activity reflects registration of episodes to memory and suggest a potential brain correlate of retroactive interference.
The function of the human hippocampus is normally investigated by experimental manipulation of discrete events. Less is known about what triggers hippocampal activity during more naturalistic, continuous experience. We hypothesized that the hippocampus would be sensitive to the occurrence of event boundaries, that is, moments in time identified by observers as a transition between events. To address this, we analyzed functional MRI data from two groups: one (n = 253, 131 female) who viewed an 8.5 min film and another (n = 15, 6 female) who viewed a 120 min film. We observed a strong hippocampal response at boundaries defined by independent observers, which was modulated by boundary salience (the number of observers that identified each boundary). In the longer film, there were sufficient boundaries to show that this modulation remained after covarying out a large number of perceptual factors. This hypothesis-driven approach was complemented by a data-driven approach, in which we identified hippocampal events as moments in time with the strongest hippocampal activity. The correspondence between these hippocampal events and event boundaries was highly significant, revealing that the hippocampal response is not only sensitive, but also specific to event boundaries. We conclude that event boundaries play a key role in shaping hippocampal activity during encoding of naturalistic events.SIGNIFICANCE STATEMENT Recent years have seen the field of human neuroscience research transitioning from experiments with simple stimuli to the study of more complex and naturalistic experience. Nonetheless, our understanding of the function of many brain regions, such as the hippocampus, is based primarily on the study of brief, discrete events. As a result, we know little of what triggers hippocampal activity in real-life settings when we are exposed to a continuous stream of information. When does the hippocampus “decide” to respond during the encoding of naturalistic experience? We reveal here that hippocampal activity measured by fMRI during film watching is both sensitive and specific to event boundaries, identifying a potential mechanism whereby event boundaries shape experience by modulation of hippocampal activity.
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