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).     

New York Prophecies: The Imaginary Future of Artificial Intelligence

The conflicts which have erupted over hacking, cracking and filesharing offer a stepping-stone for rethinking the involvement of users in innovation processes. As technical design processes invariably proceed in the shadow of established relations of social power, we can expect them to encompass conflicts over what constitutes the creative use of technology versus its misuse. The figure of the misuser calls attention to the importance of antagonistic relations in the mutual shaping of technology and society. Constructivist STS research has been criticised for neglecting the importance of antagonistic relations in favour of an emphasis on the limitless mutability of human/machine hybrids. The transformative effects of innovation processes on interests and subjectivities cannot be denied. But the induction of such transformations might be interpreted as a method through which struggles are conducted. This dynamic is particularly forthcoming in the case of filesharing, where users innovate precisely in order to overthrow the material practices upon which intellectual property law is founded. It is the intervention of law enforcement agencies in the process of drawing the line between users and misusers that makes the presence of an antagonistic relation manifest.     

Remembering talk: Individual and gender differences in reported speech

This study examined individual and group differences in the nature and frequency of reports of past speech in the autobiographical memories of young adults. A sample of 108 participants (60 females, 48 males) responded in writing to six memory prompts. They also completed the Five Factor Inventory (Costa & McCrae, 1992) and the Personal Attributes Questionnaire (Spence & Helmreich, 1978). The frequency with which participants used reported speech was correlated with agreeableness, openness, and expressivity; however, regression analyses indicated that narrators’ gender alone was the best predictor. Females used more reported speech than did males. The findings suggest that recollections of past speech are an under-appreciated yet important component of autobiographical memory.     

Comparing two perceived characteristics of autobiographical memory: Memory detail and accessibility

Four samples of participants recalled autobiographical memories. While some evidence emerged from regression analyses suggesting that judgements of the amount of detail contained in each memory and judgements of the ease with which events could be recalled were partially independent, the analyses generally showed that these judgements were similarly predicted by various event characteristics (age, typicality, self-importance, emotional intensity at event occurrence, rehearsal types). Co-occurrence frequency data yielded similar conclusions, showing that while ease ratings and detail ratings occasionally diverged, they were more often consistent with each other. Finally, the data also suggested that events that prompted emotional ambivalence were not judged to be more easily recalled, or to contain more detail, than non-ambivalent events.     

Phenomenology of autobiographical memories: The Memory Experiences Questionnaire

The phenomenology of autobiographical memories varies on a number of dimensions: some memories are vivid and others dim; some are emotionally intense and others lack emotional content. The present research sought to develop a psychometrically-sound scale to assess the entire range of dimensions on which autobiographical memories differ. We reviewed the literature on memory experiences and identified 10 relevant dimensions: Vividness, Coherence, Accessibility, Time Perspective, Sensory Details, Visual Perspective, Emotional Intensity, Sharing, Distancing, and Valence. We constructed a comprehensive item pool to assess these dimensions and, using data from several large samples (Ns=941; 510; 212), we showed that: (a) all 10 scales had adequate reliability (median alpha=.87; range=.72 to .97), (b) the 10-factor structure provided a good fit to the data, and (c) gender, personality, and memory recency had theoretically meaningful relations with the 10 scales. For example, gender and ethnicity differences in phenomenology were mediated by memory content, and early and recent memories had distinct phenomenologies. The discussion focuses on the theoretical and practical utility of the 10 scales.     

Examining the long-term stability of overgeneral autobiographical memory

Overgeneral autobiographical memory (OGM) is a proposed trait-marker for vulnerability to depression, but relatively little work has examined its long-term stability. This study investigated the stability of OGM over several years in 271 late adolescents and young adults participating in a larger longitudinal study of risk for emotional disorders. The Autobiographical Memory Test (AMT) was administered twice, with test–retest intervals ranging from approximately 3 to 6 years. There was evidence of significant but modest stability in OGM over several years. Specifically, Spearman rank correlations (ρs) between the proportions of specific and categoric memories generated on the two AMTs were .31 and .32, respectively. We did not find evidence that the stability of OGM was moderated by the length of the test–retest interval. Furthermore, the stability coefficients for OGM for individuals with and without a lifetime history of major depressive disorder (MDD) were relatively similar in magnitude and not significantly different from one another (ρs=.34 and .42 for the proportions of specific and categoric memories for those with a history of MDD; ρs=.31 for both the proportions of specific and categoric memories for those without a history of MDD). Implications for the conceptualisation of OGM are discussed.     

Social Innovation: Enhancing Creative Performance Through Causal Analysis

ABSTRACT

Prior qualitative research has indicated that social innovation, the generation and implementation of new ideas about social relationships and social organization, requires active analysis of the causes operative in a social system. To provide some quantitative evidence bearing on this proposition, 180 undergraduates were presented with six social innovation problems drawn from the business and educational domains. Training in the analysis of causes was provided and manipulations were made to induce analysis through distancing and forecasting. It was found that induction of causal analysis through training and distancing contributed to the originality of obtained problem solutions especially in less familiar domains. The implications of these findings for understanding social innovation are discussed.     

Orienting Under Load: Intrinsic Dynamics and Postural Affordances for Visual Perception

Orientation toward one's surroundings is necessary for prospective control of action, and constraints on orienting activity have consequences for animal survival. Physically coupled load is a constraint for humans wearing protective equipment (firefighters, soldiers, etc.). The consequences of load on postural affordances while transitioning to upright stance was used to quantify the impact of different soldier configurations. Eight participants established upright posture in 4 relevant load configurations (5.0 to 79.2 lb). Load affected the accessibility of optical information at a distance as evidenced by increasing downward head angles and reductions in postural coordination. Reductions in the variability of time to establish upright stance with load suggests a loss of functional adaptability. Load asymmetries played a significant role as the most asymmetric configuration (not the heaviest) had the most detrimental effect on postural affordances. Center of Pressure (CoP) dynamics reflected the consequences of asymmetric loading on postural regulation as greater power and fluctuations across frequencies were observed. Physically coupled load induces significant constraints on orienting activity, and load asymmetry contributes significantly to the detrimental effects of protective equipment on action-perception coupling during whole-body movements.