Memories for past events are highly complex, allowing us to travel back in time and subjectively re-experience episodes in our lives. These events are not stored and played back to us as we experienced them; rather, they are reconstructed in a hierarchical manner. Episodic reconstruction is thought to be facilitated by hippocampal-neocortical processes that rebuild the rich content and quality of past events within a spatio-temporal framework (Barry and Maguire, 2019; Ranganath, 2010; Ritchey et al., 2015a; Robin, 2018) and integrate them with prior knowledge (Morton et al., 2017). In turn, this adaptive, reconstructive process can lead to forgetting of specific event features and variability in the precision with which different features are remembered (Schacter et al., 2011).

Previous research has found widespread increases in cortical and subcortical brain activity when people successfully remember rather than forget events (Rugg and Vilberg, 2013). Beyond changes in activity, large-scale brain networks increase their communication strength during episodic retrieval tasks (Fornito et al., 2012; Robin et al., 2015; Westphal et al., 2017), where functional connectivity, particularly of the hippocampus, is increased when events are remembered compared to forgotten (Geib et al., 2017a; King et al., 2015; Schedlbauer et al., 2014; St Jacques et al., 2011). Such neural changes are validated by behavioral evidence showing that event features are dependent on one another in memory, emphasizing that remembering involves the binding of distinct elements into a single, coherent event representation (Horner and Burgess, 2013; Horner and Burgess, 2014). This binding process is widely thought to be facilitated by the hippocampus (Barry and Maguire, 2019; Horner et al., 2015; Moscovitch et al., 2016; Ritchey et al., 2015a). Therefore, episodic retrieval is likely dependent on the coordination of memory ‘hubs’ such as the hippocampus with neocortical regions to reconstruct and integrate the diverse components of memory representations.

Despite this research, little is known about how changes in hippocampal-cortical communication flexibly support the multidimensional quality of remembered events. Distinct cortical areas support the different building blocks of episodic memory: for instance, parahippocampal cortex (PHC) is thought to provide the hippocampus with spatial context information, whereas perirhinal cortex (PRC) codes for items within this context (Davachi, 2006; Diana et al., 2007; Diana et al., 2010; Staresina et al., 2013; Staresina et al., 2011). Moreover, these medial temporal cortical regions are situated within two large-scale networks (Ranganath and Ritchey, 2012; Ritchey et al., 2015a). These networks show functional separation but some common hippocampal connections (Kim et al., 2018; Libby et al., 2012; Ritchey et al., 2014; Wang et al., 2016), and have been proposed to support complementary memory functions. The PHC is part of a posterior-medial (PM) system thought to form situation models of events (Ritchey et al., 2015a). PM regions include retrosplenial cortex, which also demonstrates representational specificity for spatial environment (Epstein, 2008), posterior cingulate, precuneus, and angular gyrus, which are recruited during subjectively vivid recollection and represent precise episodic context information (Baldassano et al., 2017; Kuhl and Chun, 2014; Richter et al., 2016; Robin and Moscovitch, 2017; Sreekumar et al., 2018). In turn, the PRC is part of an anterior-temporal (AT) system supporting item and emotional associations (Ritchey et al., 2015a). Within this system, the amygdala binds item-specific features with emotion (Kensinger et al., 2011; Yonelinas and Ritchey, 2015), and anterior ventral temporal cortex and lateral orbitofrontal cortex are further involved in processing object representations and the affective significance of items to inform decision making and memory (Libby et al., 2014; Rolls and Grabenhorst, 2008).

A core tenet of the PMAT framework is that cortical systems must interact with each other and with the hippocampus to support the multidimensional nature of episodic memory. However, several aspects of this crucial principle have yet to be directly tested: First, how do functional network connections reorganize during episodic retrieval? Second, do changes in these connections relate to the amount and quality of information bound within memory? Finally, do different patterns of network connectivity changes support the fidelity of different types of memory content? In this study, we tested these questions to determine how cortico-hippocampal networks flexibly coordinate the reconstruction of complex events.

The contribution of network interactions to the phenomenology of memory has been difficult to establish in part due to the nature of memory tests commonly used in conjunction with functional connectivity methods, which have typically relied on binary measures of ‘successful’ retrieval or subjective ratings of vividness. These methods are insensitive to the diversity of integrated content and objective precision of retrieved events. To this end, we tested participants on a memory reconstruction task to obtain continuous measures of different episodic memory features (Brady et al., 2013; Harlow and Yonelinas, 2016; Nilakantan et al., 2017; Richter et al., 2016). Participants learned a series of objects, each with a color, scene location, and emotion association, and then reconstructed the visual appearance of the objects later on. Here, they selected a color from a continuous spectrum and moved around 360° panorama scenes to place the object in its original location, providing a sensitive, objective, and naturalistic way of assessing memory (cf. Serino and Repetto, 2018). We predicted that PM and AT systems would show a distinct network structure during encoding, but that, crucially, these networks would become more integrated during episodic retrieval. Moreover, we expected that increased inter-network and hippocampal connectivity would dynamically track binding and the composite quality of features within memory. In line with the representational organization of the PMAT framework, we finally predicted that functional connectivity of PM and AT systems would track memory precision for spatial context and item information, respectively.

Participants completed an episodic memory task in which they learned three features associated with trial-unique objects: a color from a continuous spectrum, a location within a panorama scene, and an emotionally negative or neutral sound (Figure 1A). In a subsequent test, participants were first cued to covertly retrieve as much information about each object as possible, and then they dynamically reconstructed each object’s color and scene location (Figure 1B), providing continuous measures of memory error in degrees (remembered feature value - encoded feature value). Using these fine-grained memory measures, we test how the content and fidelity of information is bound into a single memory representation, and if these memory processes are supported by flexible engagement of the PM and AT cortico-hippocampal networks (Ritchey et al., 2015a).

Figure 1

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Episodic features are recollected with varying precision

We first evaluated behavioral performance to quantify memory variability, both in terms of the probability of successful retrieval and precision of each reinstated feature. The proportion of ‘correct’ responses (memory success) was calculated for each of the object features - item color, spatial context, and emotion association - and the precision of correct retrieval was additionally estimated for color and spatial features. Here memory performance was evaluated by fitting a mixture model (Bays et al., 2009; Zhang and Luck, 2008) to each participant’s response errors (Figure 2A; see Materials and methods). Participants remembered the features well above chance on average (Table 1), and the proportion of correct responses did not differ between color and scene features (t(27) = 1.09, p=0.29). Participants varied in the precision with which they could remember these visual details, but were more precise when remembering the object’s spatial location compared to color (t(27) = 6.48, p<0.001).

Table 1

Feature	Memory success	Memory precision
Emotion	0.76 (0.02)	---
Color	0.67 (0.04)	5.40 (0.49)
Scene	0.64 (0.04)	27.00 (3.30)

Table 1—source data 1

Feature Memory Success and Precision.

https://doi.org/10.7554/eLife.45591.004

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Figure 2

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Figure 2—source data 1

Feature Errors.

https://doi.org/10.7554/eLife.45591.006

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Figure 2—source data 2

Feature Memory Dependency.

https://doi.org/10.7554/eLife.45591.007

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Memory retrieval reduces modularity and increases inter-network background connectivity

It remains untested how hippocampal, PM, and AT networks change in their communication during episodic retrieval, and how such changes contribute to episodic memory. Our neuroimaging analyses target this question in a hierarchical manner, testing i) how background network connectivity reorganizes between encoding and retrieval, ii) if dynamic changes in network communication track a measure of multidimensional memory quality, and iii) if dissociable connections support the fidelity of different types of episodic features. We first compared functional connectivity during remember events with connectivity during encoding events. Using the CONN toolbox (Whitfield-Gabrieli and Nieto-Castanon, 2012), HRF-weighted correlations between each ROI (Figure 3A) times series were computed across encoding and remember task events after first regressing out all trial- and memory-related activity and nuisance variables such as motion (see Materials and methods). Thus, connectivity within each task reflects background covariation in ROI activity independent of trial and behavioral factors driving changes in region-specific activity.

Figure 3

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Network Modularity and Density.

https://doi.org/10.7554/eLife.45591.009

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Modularity during each task was calculated from each subject’s thresholded (r >= 0.25), weighted connection matrix using the Louvain method of community detection. This algorithm calculates a global modularity value (Q), reflecting the degree to which a set of ROIs are functioning as distinct modules. PM and AT systems appeared to be functioning as relatively distinct networks during encoding (Figure 3C), but modularity across our ROIs was significantly reduced during episodic retrieval (t(27) = −3.30, p=0.003), suggesting an increase in inter-network communication and a less segregated network structure (Figure 3B). To quantify changes in within-network and between-network communication, mean network density (strength of connections) was calculated for all ROI pairs within the same hypothesized network and for all ROI pairs in different networks. Supporting our a priori network structure, ROIs within the same network had substantially stronger connectivity strength than ROIs between networks (F(1,27) = 132.83, p<0.001). Episodic retrieval was accompanied by an overall increase in connectivity strength relative to encoding (F(1,27) = 14.84, p<0.001), although the change in between-network connectivity was disproportionately greater than change in within-network connectivity (F(1,27) = 11.43, p=0.002). Of note, change in modularity between encoding and retrieval and the disproportionate increase in between-network connectivity strength was robust to different thresholds used to define connections (modularity ts >3.18, ps<0.004; network density interaction Fs > 10.47, ps<0.003; see Materials and methods). Therefore, episodic retrieval is characterized by a notable increase in inter-network connections of hippocampus, PM, and AT regions, and a breakdown in a modular network structure, perhaps facilitating integration of different event features during memory reconstruction.

Dynamic changes in hippocampal-cortical network connectivity predict memory quality

The background connectivity results suggest that episodic retrieval is associated with a less modular hippocampus, PM, and AT network structure, consistent with prior research (Westphal et al., 2017). Yet it is unclear whether these changes in network connectivity reflect a general retrieval state or whether they actually support the recovery of complex episodic information. To address this question, we used generalized psychophysiological interaction (gPPI) analyses to measure how effective connectivity of each ROI pair might be modulated by an event-specific, continuous measure of multidimensional memory quality. This measure captures fine-grained information bound in memory, accounting for both the amount and precision of remembered features (see Materials and methods), thus providing a measure of retrieval sensitive to the quality and diversity of memory content. Note that gPPI measures the influence of a seed on a target region after partialling out task-unrelated connectivity and task-related activity, and thus the results include an asymmetrical effective connectivity matrix.

Averaging across all possible ROI pairs, as predicted, there was an overall increase in connectivity with event-specific increases in memory quality (mean beta = 0.36, SE = 0.16; t(27) = 2.17, p=0.019). Taking the average of within-network and between-network connections for each seed-to-target pair, we next tested how connectivity across our networks changed with increasing quality of remembered details (Figure 4A). In line with the results of the background connectivity analyses, it was primarily connections between our networks, particularly with the hippocampus, that increased with memory quality. Specifically, AT-PM connectivity increased with higher memory quality (ts(27) > 1.96, ps<0.05, FDR-corrected), and both the AT (t(27) = 3.10, p=0.007, FDR-corrected) and PM (t(27) = 3.29, p=0.007, FDR-corrected) networks increased their connectivity to hippocampus. In tests of the other direction, the hippocampus seed increased its connectivity to the PM system (t(27) = 2.39, p=0.027, FDR-corrected), but not significantly so to the AT system (t(27) = 1.65, p=0.06). This unidirectional hippocampus-AT relationship implies that AT system activity explains more variance in hippocampal activity with greater memory quality, but not vice versa. Turning to within-network connections, anterior and posterior hippocampus increased their connectivity with each other with better memory (t(27) = 3.12, p=0.007, FDR-corrected), but there was only a small change in within-PM connectivity (t(27) = 1.71, p=0.049, uncorrected) and no significant change in within-AT communication (t(27) = 0.73, p=0.235). The individual ROI-to-ROI connections that showed a significant increase in connectivity with memory quality are shown in Figure 4B. Of note, when comparing objects that had been associated with an emotionally negative or neutral sound, increases in network connectivity with memory quality appeared to be slightly stronger for negative-associated objects, most predominantly for within-PM connections (t(27) = 2.24, p=0.033 uncorrected), and AT-to-PM connections (t(27) = 2.74, p=0.011 uncorrected), although these emotion effects did not survive correction for multiple network comparisons.

Figure 4

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Memory-Modulated Hippocampal Connectivity.

https://doi.org/10.7554/eLife.45591.011

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Figure 4—source data 2

Memory-Modulated ROI Activity.

https://doi.org/10.7554/eLife.45591.012

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Exploring these memory-related changes in hippocampal-cortical network connectivity in more detail, we compared anterior and posterior hippocampus: Is there differential connectivity change with the PM and AT systems along the hippocampal long axis? Comparing the mean of bidirectional memory-modulated connectivity between each hippocampal subregion and cortical network revealed no differences between aHipp and pHipp, as well as no differences in connectivity change with the AT and PM systems, and no interaction between these factors (Fs(1,27) < 1.96, ps>0.17) (Figure 4C). At the individual region level, there were also no significant differences between pHipp and aHipp in terms of change in connectivity strength with increasing memory quality (|ts| < 2.34, ps>0.26, FDR-corrected). In an exploratory, post-hoc test, we re-ran these analyses using only the most posterior half of pHIPP and the most anterior half of aHIPP to probe if our results might have been a function of how we subdivided the hippocampus. Interestingly, there was still no interaction between hippocampal subregion and network (F(1,27) < 0.01, p=0.94), but across both networks, connectivity changes were significantly greater for pHIPP than aHIPP (F(1,27) = 5.46, p=0.027). Therefore, we found some evidence for differences along the hippocampal long axis, at least in the most extreme segments; compared to aHipp, pHipp exhibited stronger increases in cortical connectivity with higher memory complexity.

Finally, we ran two control analyses to test the role of our ROIs in supporting episodic memory quality. First, to determine whether increases in hippocampal synchrony were specific to our networks of interest or whether evident globally, we analyzed whole-brain connectivity changes with memory. Here, we evaluated the main effect of pHipp and aHipp seeds in terms of the modulatory effect of memory quality on seed-to-voxel connectivity (see Figure 3D). The hippocampus increased its communication with voxels in a select group of brain regions, including left dorsolateral prefrontal cortex (−54, 18, 40, k = 784), bilateral parietal cortex (left: −36,–68, 42, k = 440; right: 40,–64, 58, k = 170), precuneus (6,–72,46, k = 437), superior frontal gyrus (multiple clusters, total k = 620), posterior cingulate (4,–28, 30, k = 186), inferior lateral occipital cortex (−50,–76, −20, k = 173), retrosplenial cortex (−2,–42, 2, k = 111), and precentral gyrus (4,–22, 82, k = 90). Second, to verify that our ROIs, particularly hippocampus, showed the expected sensitivity to memory retrieval in our task, we ran a univariate general linear model in which remember events were parametrically modulated by trial-specific values of memory quality. As expected, mean activity of a number of ROIs, particularly within the PM network and hippocampus, positively tracked the quality of episodic retrieval (Figure 4E). Surprisingly, unlike other PM regions, the relationship between angular gyrus activity and memory quality was not significant. However, this is likely to be a function of our use of bilateral ROIs to assess network-wide connectivity, where memory effects are more pronounced in left ANG (Rugg and King, 2018). The present connectivity analyses control for changes in region-specific activity with memory, thus highlighting the additional importance of functional communication of the PM and AT systems and hippocampus to episodic retrieval.

Dissociable PMAT connections predict the precision of recalled item and spatial features

The analyses of multidimensional memory quality provide evidence that changes in PM and AT inter-network communication, particularly with hippocampus (cf. Fornito et al., 2012; Geib et al., 2017b; King et al., 2015; Schedlbauer et al., 2014), positively track the complexity of information bound within memory. Yet, because this measure is a composite of the quality of all memory features, it remains unknown how PMAT connections support the fidelity of different types of remembered information. This is particularly important to address in light of existing frameworks that emphasize the role of informational content in determining memory organization (Davachi, 2006; Diana et al., 2007; Eichenbaum et al., 2012; Graham et al., 2010). In the medial temporal lobes and connected areas (Ranganath and Ritchey, 2012; Ritchey et al., 2015a), AT regions are sensitive to item-specific associations, and PM regions are sensitive to contextual information, but it is unclear how this organization emerges in terms of network interactions. To this end, we further focused on remember events, specifically trials where a feature was ‘successfully’ recalled, and tested where changes in connectivity tracked increasing precision of event-specific i) item color and ii) spatial context, given that these measures were found to be independent in memory (see Behavioral Results).

Looking at the average change in connectivity across every seed-to-target pair, we found that there was an overall positive change in connectivity with the precision of both item-color (mean beta = 0.24, SE = 0.11; t(27) = 2.11, p=0.022) and spatial memory (mean beta = 0.25, SE = 0.13; t(27) = 1.94, p=0.032). Are these overall increases in connectivity driven by distinct patterns? Interestingly, within-subject correlations between color and spatial ROIxROI gPPI matrices revealed no evidence for a similar pattern of connectivity changes with memory precision for these features (mean z = 0.02, SE = 0.04; t(27) = 0.50, p=0.312). At the network level (Figure 5A), higher color precision in memory was associated with increased connectivity from the AT system to the hippocampus (t(27) = 2.24, p=0.017), between the hippocampus and PM system (ts(27) > 1.82, ps<0.04), as well as increased communication between the AT and PM systems (ts(27) > 2.04, ps<0.026). All other changes in connectivity were not significant (ts(27) < 1.48, ps>.074). Of note, these individual network effects were relatively small and did not survive FDR-correction, although marginal. This may be partially explained by a significant modulatory effect of emotional valence: Objects with a negative association showed more pronounced changes in connectivity with increasing color precision than objects encoded with a neutral sound association (t(27) = 2.34, p=0.027). In contrast to the color precision results, higher spatial precision in memory was accompanied by increased communication strength within the PM system (t(27) = 2.88, p=0.018, FDR-corrected) as well as from the AT to the PM system (t(27) = 2.87, p=0.018, FDR-corrected). No other network-level connectivity changes were significant (ts(27) < 1.65, ps>0.06, uncorrected), and these effects were not modulated by the valence of the object’s emotion association (t(27) = −0.32, p=0.75). Therefore, item-color precision and spatial precision in memory were associated with dissociable network connectivity patterns, and these patterns included an increase in inter-network AT connectivity and hippocampal communication for item-color, but an increase in within-PM connectivity and no change in hippocampal communication for spatial information.

Figure 5

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Feature-Related Connectivity.

https://doi.org/10.7554/eLife.45591.014

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Finally, to identify ROI connections that might be contributing to these feature-related network patterns, analyses were further restricted to focus on four seed regions that we hypothesized should show the most representational specificity within our experimental paradigm, including 2 AT regions - PRC and AMYG - and 2 PM regions - PHC and RSC (Figure 5B). These regions show the most reliable findings of specificity to (i) item-feature and item-emotion bindings and (ii) spatial representations, respectively (Epstein, 2008; Kensinger et al., 2011; Ritchey et al., 2019; Robin et al., 2018; Staresina et al., 2011) and are core representational nodes of the PMAT systems (Ritchey et al., 2015a). We tested how these seed regions changed their connectivity to all other regions with (i) increasing color memory precision and (ii) increasing spatial memory precision. All statistics were FDR-corrected. For color precision, PRC showed the most widespread changes in connectivity to aHipp, PREC, and ANG (ts(27) > 2.38, ps< 0.045). Additionally, AMYG increased its connectivity with PREC (t(27) = 2.84, p=0.046) and PHC increased its communication with pHipp (t(27) = 2.85, p=0.046). In contrast, the most pronounced increases in connectivity with spatial precision involved PM regions: RSC increased its connection with ANG, PREC, and PCC (ts(27) > 2.91, ps< 0.013), PHC with ANG and PCC (ts(27) > 2.99, ps< 0.016), and PRC increased its communication with ANG (t(27) = 2.91, p=0.040). Because both sets of seeds showed precision-related changes in connectivity with ANG and PREC, two regions previously associated with the vividness and precision of episodic recollection (Lee et al., 2018; Oedekoven et al., 2017; Richter et al., 2016; Sreekumar et al., 2018), we ran post-hoc tests to further investigate if PM seed (PHC and RSC) and AT seed (PRC and AMYG) connections to these common targets differed by feature (Figure 5C). The change in connectivity of PM seeds to ANG/PREC was significantly greater for spatial than color precision (t(27) = 2.67, p=0.013), but there was no difference between the features in connectivity of AT seeds (t(27) = 0.10, p=0.92). Therefore, although there is notable overlap in the PMAT connections that contribute to the precision of different features in memory, there appears to be a degree of representational specificity in connectivity patterns.

Much research has demonstrated widespread increases in functional connectivity during episodic retrieval (Fornito et al., 2012; Geib et al., 2017a; King et al., 2015; Schedlbauer et al., 2014; St Jacques et al., 2011; Westphal et al., 2017), yet how these changes relate to the phenomenology of recollective experience has remained unknown. The complex process of recollection is associated with several distinct elements, including subjective feelings of vividness, as well as the number of details recalled, types of details recalled, and the precision of that information. Here, we focus on the neural dynamics supporting the content and precision of recollected information. While several prominent accounts have posited that medial temporal regions, including PHC and PRC, provide memories with complementary spatial and item-specific representations, respectively, (Davachi, 2006; Diana et al., 2007; Eichenbaum et al., 2012; Graham et al., 2010), a recent model - the PMAT framework - extends this representational sensitivity to large scale cortical networks (Ranganath and Ritchey, 2012; Ritchey et al., 2015a). Here, a PM system provides the spatial contextual scaffold for event details, including item, emotional, and semantic information provided by an AT system. This content is thought to be integrated as an event via the hippocampus (Barry and Maguire, 2019; Moscovitch et al., 2016). Although a core prediction of the PMAT framework is that functional interactions between cortical systems and the hippocampus are crucial for reinstating multidimensional episodic information, this prediction has not before been tested. First, we found that the PMAT cortical systems functioned in a modular way during memory encoding, with the hippocampus connecting to both systems. In contrast, episodic retrieval was accompanied by a disproportionate increase in inter-network connections. Second, we found that both cortical systems dynamically increased their connectivity to hippocampus with increasing multidimensional quality of episodic memory. Finally, we found that color and spatial memory precision did not clearly map on to changes in AT and PM connectivity, respectively, but rather that feature-related differences emerged in how the networks communicated with each other and with the hippocampus.

Previous research has reliably demonstrated functional segregation of the PMAT systems during rest (Libby et al., 2012; Ritchey et al., 2014; Wang et al., 2016). Here, we observe a similarly clear pattern of modularity with background connectivity during memory encoding, thus extending evidence for this network structure to directed cognition. Interestingly though, this structure was less pronounced during episodic retrieval, which was associated with an increase in between-network connections, supporting the idea that reinstatement of event representations is likely driven by interactions of the hippocampus and cortical regions and between cortical systems. Reduced modularity during memory retrieval has been previously demonstrated at the whole-brain level alongside increased hippocampal connectivity (Geib et al., 2017b; McCormick et al., 2015; Westphal et al., 2017). Enhanced connectivity between large-scale cortical systems, including default mode and frontoparietal control networks, during episodic memory retrieval has also been shown (Fornito et al., 2012; Kragel and Polyn, 2015; Robin et al., 2015; St Jacques et al., 2011; Westphal et al., 2017). However, none of these prior studies directly compared whole-brain or network-level connectivity during retrieval and encoding. Our finding of greater functional coupling of the PMAT cortical systems and hippocampus during episodic retrieval thus complements this previous work and serves as a necessary foundation for understanding how the retrieval process alters network dynamics.

Extending evidence of PMAT-hippocampal integration during retrieval, we found that connectivity between these networks further tracked the event-specific quality of memory. Previous research has found that increased functional communication, particularly with hippocampus, seems to be important for ‘successful’ episodic retrieval (Geib et al., 2017b; King et al., 2015; Schedlbauer et al., 2014). Results of our whole-brain connectivity analysis showed that the hippocampus increased its interaction with a select group of regions, most notably posterior medial and left lateral frontal regions, showing a similar pattern to the results of King et al. (2015). In prior studies, memory on each trial has been typically quantified in terms of retrieving or forgetting a single episodic feature or a subjective judgment of recollection, thus neglecting the multidimensional quality of event representations. Here, we used a composite score including information about the number of features present in memory as well as quality of those features. This allowed us to show that inter-network connectivity changes parametrically capture an objective level of memory detail rather than just the process of retrieval. Increased connectivity of PMAT regions to the hippocampus with multidimensional memory quality strongly suggests that hippocampal-cortical connections may specifically act to bind multiple sources of event-specific information together in memory (Diana et al., 2007; Horner et al., 2015; Ranganath, 2010), supporting flexible content retrieval (Horner and Doeller, 2017), rather than simply facilitating access to individual associations or providing a general index of recollection. Although we did not find evidence for differences in memory-related network connectivity between our a priori anterior and posterior hippocampal subregions, an exploratory analysis revealed differences between the most extreme long axis segments. Posterior hippocampus showed stronger increases in memory-related connectivity than anterior hippocampus, but there were no network-specific differences in connectivity patterns. This result aligns with recent findings of increased representational granularity along the human hippocampal long axis (Brunec et al., 2018; Nadel et al., 2013; Poppenk et al., 2013; Sheldon et al., 2016), such that posterior hippocampus might play a greater role in reconstructing detailed, precise episodic information by integrating AT and PM systems.

Our behavioral results additionally revealed new evidence that episodic memories are bound at a level that includes the gist of recovered information, but not necessarily the exact precision with which it is remembered. Successful retrieval of episodic information showed the expected dependent structure of a hippocampal binding process (Horner and Burgess, 2013; Horner and Burgess, 2014), such that retrieving one feature facilitated memory for the others. This was particularly the case for spatial associations, such that successful retrieval of spatial location was associated with better memory for the other features, supporting the organizational role of space in memory (Robin, 2018). Interestingly, the precision of each individual feature was at least partially independent of this binding mechanism, such that retrieving a scene location did not significantly improve the precision of color memory, and vice versa, and the precision of recollected item color and spatial context was also unrelated. These results align with the perspective that the primary role of the hippocampus is to bind event features into a coherent spatio-temporal representation but the quality of individual event features occurs at the level of cortical representations (Barry and Maguire, 2019). Therefore, the precision of bound features is theoretically separable from the binding process itself (cf. Richter et al., 2016). Other accounts have emphasized the role of the hippocampus in supporting high-resolution bindings, but these studies have typically focused on the precision of a single association (Kolarik et al., 2018; Nilakantan et al., 2018; Yonelinas, 2013). Thus, the present results question whether there are limits to the precision of hippocampal representations, driven by either the number of multimodal episodic associations or the type or precision of individual associations (Yonelinas, 2013).

The current study design additionally allowed us to examine functional connectivity changes associated with the precision of distinct features within memory. We expected that within-PM and PM-hippocampal communication would increase with spatial precision, whereas within-AT and AT-hippocampal communication would increase with item color precision. Our results partially supported these predictions: inter-network connectivity of the AT system, hippocampus, and PM system tracked the precision of item color memory, whereas connectivity to and within the PM system tracked the precision of scene location memory. In line with our hypotheses, connectivity among PHC, RSC and dorsal PM regions scaled with the precision of spatial but not color memory, suggesting that within-PM connectivity might selectively support the resolution of spatial context associations. Much research has documented the complementary roles role of PHC and RSC in spatial processing and navigation (Epstein, 2008; Mitchell et al., 2018), including sensitivity to distance within virtual environments (Sulpizio et al., 2014). Moreover, a recent study showed that RSC is important for forming scene representations and is sensitive to the identity of specific views in 360° panorama scenes (Robertson et al., 2016), in line with its role in viewpoint precision demonstrated here. Surprisingly, we found no evidence that hippocampal connectivity supported the precision of PM spatial representations, which is in contrast to evidence implicating the hippocampus, particularly posterior, in spatial precision specifically (Nadel et al., 2013; Nilakantan et al., 2017; Nilakantan et al., 2018; Stevenson et al., 2018).

In contrast, color precision was associated with connections between AT regions, particularly PRC, to PM regions and hippocampus. Involvement of the PRC complements previous findings that activity of this region is sensitive to item and item-color bindings in memory (Diana et al., 2010; Staresina and Davachi, 2008). However, the finding that item-color precision was related to inter-network connectivity, rather than within-AT connectivity, was an unexpected result. There are two possible explanations: First, during episodic reconstruction, the fidelity of item representations may be necessarily integrated within a broader PM contextual framework via the hippocampus. This could explain why hippocampal connectivity supported the precision of color but not necessarily spatial associations in memory. However, color memory precision was not significantly dependent on retrieval of the scene location in our study, providing a tentative argument against this interpretation. Alternatively, the angular gyrus and precuneus may play a content-general role in the retrieval and representation of high-fidelity information, thus explaining increased AT-PM connectivity associated with item-color precision. Previous research has demonstrated consistent involvement of these regions in the representation of subjectively vivid and objectively precise information during memory retrieval using both univariate activation and multivariate methods (Lee et al., 2018; Oedekoven et al., 2017; Richter et al., 2016; Sreekumar et al., 2018). Moreover, anterior-posterior neural contributions to memory have been proposed to follow a specificity gradient, from low resolution to high resolution representations respectively, and not strictly based on informational content (Robin and Moscovitch, 2017). Our findings lend some support to both perspectives: We find evidence for anterior-posterior content sensitivity in terms of the most influential seed regions, but also common functional projections to angular gyrus and precuneus supporting precise memory retrieval.

The present study revealed network connectivity changes associated with the precision of different features during the same retrieval event, indicating that parallel changes in network dynamics support the complexity and content of episodic memory. Future research should examine the specificity of these cortico-hippocampal connections more closely, for instance, using causal methods that can adjudicate their specific contributions (Kim et al., 2018; Nilakantan et al., 2017). These methods will be particularly useful given that episodic memories by definition reflect an integrated structure of item and context information. As such, our data show involvement of AT-PM connections, including PRC and PHC seeds, in the precision of both item color and scene location memory, and some prior research has highlighted engagement of PRC and PHC during recall of both object and spatial information (Burke et al., 2018; Ross et al., 2017). Future research should also account for the temporal evolution of episodic memory, both in terms of the event itself and the retrieval process. For instance, research has found shifting hippocampal connectivity patterns between memory search and elaboration (McCormick et al., 2015; St Jacques et al., 2011), and it is an open question how this temporal change would apply to the hippocampal-PMAT connections discussed here. In summary, we provide evidence that PM and AT cortical systems increase their functional communication with each other and hippocampus during episodic retrieval, dynamically increasing with the level of multidimensional memory quality. Moreover, we demonstrate for the first time how these connections support the fidelity of complementary representations, driving the flexible reconstruction of past events.

Data and code have been made available via GitHub: https://github.com/memobc/paper-orbitfmri (copy archived at https://github.com/elifesciences-publications/paper-orbitfmri).

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Author details

1. Rose A Cooper

   Department of Psychology, Boston College, Boston, United States

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   rose.cooper@bc.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1521-8371

2. Maureen Ritchey

   Department of Psychology, Boston College, Boston, United States

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5957-3642

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