Time-dependent transformations of memory representations differ along the long axis of the hippocampus

Research has shown that sleep is beneficial for the long-term retention of memories. According to theories of memory consolidation, memories are gradually reorganized, becoming supported by widespread, distributed cortical networks, particularly during postencoding periods of sleep. However, the effects of sleep on the organization of memories in the hippocampus itself remains less clear. In a 3-d study, participants encoded separate lists of word–image pairs differing in their opportunity for sleep-dependent consolidation. Pairs were initially studied either before or after an overnight sleep period, and were then restudied in a functional magnetic resonance imaging (fMRI) scan session. We used multivariate pattern similarity analyses to examine fine-grained effects of consolidation on memory representations in the hippocampus. We provide evidence for a dissociation along the long axis of the hippocampus that emerges with consolidation, such that representational patterns for object–word memories initially formed prior to sleep become differentiated in anterior hippocampus and more similar, or overlapping, in posterior hippocampus. Differentiation in anterior hippocampal representations correlated with subsequent behavioral performance. Furthermore, representational overlap in posterior hippocampus correlated with the duration of intervening slow wave sleep. Together, these results demonstrate that sleep-dependent consolidation promotes the reorganization of memory traces along the long axis of the hippocampus.

The hippocampus has long been considered critical for encoding new memories; however, the effects of consolidation on hippocampal memory traces has remained an area of active research. Memories are thought to be stabilized for the long term as they become distributed across neocortical networks (Buzsáki 1989; Alvarez and Squire 1994; McClelland et al. 1995), a process supported by mechanisms during sleep (Diekelmann and Born 2010; Rasch and Born 2013). Whereas much research has been devoted to understanding the hippocampal contributions to the long-term retention of memories, open questions remain in considering how sleep-dependent consolidation affects the organization of hippocampal traces.The hippocampus has previously been shown to be critical for binding disparate elements of an experience together (Cohen and Eichenbaum 1993; Davachi 2006). Theories suggest that the hippocampus quickly encodes new experiences, while the cortex, with a slower learning rate, gradually comes to represent the central features from this hippocampal trace, resulting in abstracted memories that can be integrated into long-term cortical stores (McClelland et al. 1995). Prior research has demonstrated evidence for a coordinated hippocampal–cortical dialogue during sleep (Andrade et al. 2011; Bergmann et al. 2012; Ngo et al. 2020) as well as enhanced hippocampal–cortical functional connectivity after learning, facilitating the retention of memories (Tambini et al. 2010; Tompary et al. 2015; Murty et al. 2017; Cowan et al. 2021). Reports suggest consolidation results in more integrated cortical memory traces in the cortex (Richards et al. 2014; Tompary and Davachi 2017; Cowan et al. 2020); however, it remains an open question whether the active consolidation processes that support memory reorganization across hippocampal–cortical networks also transform hippocampal memory traces.Research on the fate of the hippocampal trace with consolidation has often focused on questions about the permanence of memories in the hippocampus. Theories of systems consolidation have classically debated whether the hippocampal trace is time-limited (Alvarez and Squire 1994), or, rather, whether the hippocampus continues to represent memories in perpetuity (Nadel and Moscovitch 1997; Winocur and Moscovitch 2011; Moscovitch et al. 2016; Sekeres et al. 2018a). Another theory posits that while the original hippocampal trace is transient, during retrieval the hippocampus reconstructs details of an experience from cortical traces (Barry and Maguire 2019). Much research in this vein has focused on investigating changes in hippocampal blood-oxygenation level-dependent (BOLD) univariate activation with time (Bosshardt et al. 2005a,b; Takashima et al. 2006, 2009; Gais et al. 2007; Sterpenich et al. 2007, 2009; Yamashita et al. 2009; Milton et al. 2011; Watanabe et al. 2012; Ritchey et al. 2015; Baran et al. 2016; Dandolo and Schwabe 2018) and the effects of hippocampal lesions in animals and humans (Winocur et al. 2001; Frankland and Bontempi 2005; Winocur and Moscovitch 2011; Moscovitch et al. 2016) with mixed results. Interestingly, pinpointing these effects along the long axis of the hippocampus has also proven unclear. Some reports have found that only the anterior hippocampus exhibits time-dependent changes in retrieval-related univariate activation, with evidence of decreases with delay (Takashima et al. 2006; Milton et al. 2011; Dandolo and Schwabe 2018), but also evidence of greater activation for more remote, compared with recent, memories (Bosshardt et al. 2005a,b). At the same time, other studies have found decreases in univariate activation only in the posterior hippocampus (Bosshardt et al. 2005b; Takashima et al. 2009; Yamashita et al. 2009; Milton et al. 2011; Watanabe et al. 2012; Ritchey et al. 2015; Sekeres et al. 2018b).Because of these conflicting findings, instead of asking just about dependence or overall changes in activation in the hippocampus, theories and empirical research have instead increasingly considered the organization of memory representations in the hippocampus (Robin and Moscovitch 2017; Sekeres et al. 2018a). Broadly, using representational similarity analyses, several studies have shown that hippocampal memory representations tend to become differentiated over learning, particularly for memories with overlapping content (LaRocque et al. 2013; Schlichting et al. 2015; Chanales et al. 2017; Brunec et al. 2020). Furthermore, it has been suggested that information is represented at different scales or “granularity” along the long axis of the hippocampus, in line with place field size differences (Kjelstrup et al. 2008; Komorowski et al. 2013), with anterior hippocampus representing more similar, coarse-grained, or gist-like information, while the posterior hippocampus represents fine-grained, detail-oriented representations (Evensmoen et al. 2013; Poppenk et al. 2013; Robin and Moscovitch 2017; Brunec et al. 2018, 2020). However, limited work has investigated whether this representational organization is altered with consolidation. Reports have shown that memory representations sharing overlapping content become more similar over a delay (Tompary and Davachi 2017; Audrain and McAndrews 2020), yet other work has found that hippocampal representations were not modulated by time (Ritchey et al. 2015; Ezzyat et al. 2018). Intriguingly, reports indicating greater differentiation in memories in anterior compared with posterior hippocampus with consolidation (Tompary and Davachi 2017; Dandolo and Schwabe 2018; Ezzyat et al. 2018) raise the possibility that the representational granularity along the anteroposterior axis may be transformed with consolidation. Thus, more work is needed to understand how consolidation influences the representational structure of memories in the hippocampus. In particular, despite much research connecting sleep to consolidation (Diekelmann and Born 2010; Rasch and Born 2013), it remains unknown whether sleep-dependent processes facilitate such delay-dependent transformations to the hippocampus.Active processes in the sleeping brain seem to be optimized for systems consolidation. Currently, the best mechanistic evidence for sleep-dependent consolidation comes from studies on hippocampal replay showing the repeated reactivation of encoding-related patterns of hippocampal activity (Buzsáki 1989; Wilson and McNaughton 1994; Girardeau and Zugaro 2011), which seems to be coordinated with replay in areas of the cortex (Ji and Wilson 2007; Peyrache et al. 2009; Wierzynski et al. 2009). It is thought that the coupling between oscillations during non-REM sleep stages (particularly slow wave sleep [SWS])—including sharp wave ripples that support replay, thalamocortical spindles, and slow oscillations—facilitates the hippocampal–cortical dialogue and information transfer to the cortex (Buzsáki 1996; Sirota et al. 2003; Steriade 2006; Clemens et al. 2011; Mölle and Born 2011; Staresina et al. 2015). Indeed, our previously published work from the present study provided supporting evidence that the density of thalamocortical sleep spindles (11–16 Hz) during overnight sleep is related to enhanced hippocampal–cortical functional connectivity measures, and increased similarity, or greater representational overlap, among memories in the ventromedial prefrontal cortex (vmPFC) (Cowan et al. 2020). Yet, while some prior work has shown that features of sleep, including spindle density and the duration of non-REM SWS, are related to decreased retrieval-related hippocampal activation for memoranda learned prior to sleep (Takashima et al. 2006; Baran et al. 2016; Hennies et al. 2016), it remains unclear how the reactivation of hippocampal traces during replay may impact the way memories are organized along the long axis of the hippocampus.To examine the effects of sleep-dependent consolidation on the neural representation of memories in the hippocampus, we designed a within-participant 3-d study using overnight polysomnography (PSG), functional magnetic resonance imaging (fMRI), and behavioral measures of memory (Fig. 1). In this study, aspects of which have been previously published (Cowan et al. 2020), participants first studied a list of word–image pairs before sleeping overnight (Sleep List), during which PSG was recorded. Upon waking in the morning, participants studied a new list of pairs (Morning List). The word–image pairs from these two lists were then restudied while undergoing an fMRI scan, intermixed with a third, novel list of pairs (Single Study List). Associative memory was tested immediately after the scan and again 24 h later. We compared measures of multivariate pattern similarity and univariate BOLD signal for the lists learned prior to, or after, sleep to probe how modulating the opportunity for sleep-dependent consolidation impacts the way memories are organized across the long axis of the hippocampus. Furthermore, our design allowed us to examine how features of overnight sleep are related to the representational organization of memories learned prior to the sleep period, as well as the behavioral benefit of changes to the organization of these memories. Thus, our study provides a novel examination of the effects of sleep-dependent consolidation on the representation of memories along the long axis of the hippocampus.Open in a separate windowFigure 1.Study design. For all encoding and restudy sessions, participants were asked to form an association between a word and an image. Participants first encoded the Sleep List (blue) before sleeping overnight while polysomnography was recorded. The next morning (day 2), participants encoded a second set of novel word–image pairs (Morning List). After a short delay (∼2 h), participants restudied these two sets of pairs, intermixed with novel pairs (Single Study List) in the functional magnetic resonance imaging (fMRI) scanner. Source memory was tested immediately after the scan and after a 24-h delay (day 3).     

The effects of relationship context and modality on ratings of funniness

There is evidence to suggest that humour is an important part of mate choice and that humour may serve as an indicator of genetic quality. The current study investigated how rated funniness from a video clip was related to an individual’s attractiveness as a short-term or long-term partner. We additionally tested for the presence of an attractiveness halo effect on humour ratings by comparing ratings of funniness from video clips, audio-only presentations, and photographs. We found that funniness was most strongly correlated with attractiveness for short-term relationships, especially in videos of males. We also found that attractiveness was related to funniness ratings differently across video, audio-only clips, and photographs. Relative to their rated funniness in the audio-only condition, with no appearance cues, attractive individuals were rated as funnier in video clips than less attractive individuals. An additional study demonstrated that ratings of flirtatiousness and funniness were strongly correlated. Perceived similarity between producing humour and flirting may explain why humour is more preferable in a short-term partner as flirting may be seen to signal proceptivity. The effects of attractiveness on humour judgement may also be explained by an association with flirtation as flirting may be most enjoyable when directed by attractive individuals.     

Individual differences in the ability to avoid distracting sounds

The present work aims to establish a greater understanding of the cognitive mechanisms involved in avoiding distraction from speech and nonspeech sounds. Although mixed results have been presented by research investigating the hypothesis that individuals with superior working memory abilities are better able to avoid acoustic distraction, we found that working memory correlated with some aspects of performance during distraction when carefully examined. This is consistent with the view that working memory involves resisting interference. In a large sample, we examined two different tasks accompanied by acoustic distraction—serial recall and rapid colour naming—as well as two different measures of working memory (operation span and running span). We show that the previous inability to find relations between working memory and avoidance of distraction may stem from the use of inadequate correlational techniques. Additionally, the level of difficulty of the serial recall task may be an important factor. The results illustrate that commonly used statistical techniques can be misleading and furthermore that the ability to avoid distraction from irrelevant items may not be a unitary construct.     

Exits and Migrations: Foregrounding the Christian Counter-Cult

Most of the scholarly work on the anti-cult movement (ACM), to the extent that it has considered the Christian counter-cult movement (CCM) at all, has subsumed it as a subtle variant of a larger phenomenon. This is problematic in that at many levels, the CCM differs substantially from the ACM. This paper examines some of the conceptual differences in order to elucidate the nature of the tension between established religions in the dominant culture (in this case, Christianity) and controversial religious groups that are perceived as intruders on the religious market place.     

Is there a temporal basis of the word length effect? A response to Service (1998)

Service (1998) carried out a study of the word length effect with Finnish pseudowords in which short and long pseudowords were identical except for the inclusion of certain phonemes differing only in pronunciation length, a manipulation that is impossible in English. She obtained an effect of phonemic complexity but little or no word duration effect per se - a discrepancy from the expectations generated by the well-known working memory model of Baddeley (1986). In the present study using English words, we controlled for phonemic complexity differences by using the same words for the short- and long-word sets, but with instructions inducing shorter or longer pronunciation of the words. We obtained substantial word duration effects. Concerns raised by Service are addressed, and we conclude that both duration and complexity are likely to contribute to the word length effect in serial recall.     

The theory of braids and the analysis of impossible figures

Impossible figures were regarded neither as new perceptual phenomena, nor as examples of known phenomena such as illusions. They were seen as geometric anomalies, not psychological ones, which serve a heuristic function in the study of perception. With this in mind, a topological analysis was undertaken with the anticipation of the following goals: (a) A systematic way (algorithm) of generating these figures should be evident; (b) simple properties of impossible figures which may not have been previously understood should be discovered. Both of these conditions were met.     

Epistemic perceptualism and neo-sentimentalist objections

Epistemic Perceptualists claim that emotions are sources of immediate defeasible justification for evaluative propositions that can (and do) sometimes ground undefeated immediately justified evaluative beliefs. For example, fear can constitute the justificatory ground for a belief that some object or event is dangerous. Despite its attractiveness, the view is apparently vulnerable to several objections. In this paper, I provide a limited defence of Epistemic Perceptualism by responding to a family of objections which all take as a premise a popular and attractive view in value theory – Neo-Sentimentalism – according to which values are analysed in terms of fitting emotions.     

A meta-analysis of aggression in the presence of violent cues: Effects of gender differences and aversive provocation

Meta-analytically examines experimental studies that include violent cues in the setting and assesses the effects of aversive provocation on gender differences in aggression. The results show that when violent cues are present, men are more aggressive than women under neutral unprovoked conditions. However, when they are exposed to both violent cues and aversive provocation, men and women are equally aggressive. Differences in individual reactivity to violent cues as well as the type of aggressive response and the sex of the target also affected the magnitude of gender differences in the presence of violent cues. Aggr. Behav. 23:447–456, 1997. © 1997 Wiley-Liss, Inc.