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Introduction
The hippocampus has long been implicated in encoding salient contexts, such as novelty and reward (Düzel, Bunzeck, Guitart-Masip, & Düzel, 2010; Nyberg, 2005; Shohamy & Adcock, 2010), and its role extends to motivational states, such as intrinsic curiosity (Gruber & Ranganath, 2019). While previous functional magnetic resonance imaging (fMRI) studies have investigated the effects of motivation on memory, they have primarily focused on the hippocampus as a whole or along its longitudinal axis (i.e., anterior vs. posterior hippocampus) (Grady, 2019; Kim, 2022; Miendlarzewska, Bavelier, & Schwartz, 2016; Robin & Moscovitch, 2017). However, these approaches have limited comparability with extant animal models of novelty- and reward-based memory, which focus on specific hippocampal subfields (Lisman & Grace, 2005). Here, we examined activity and multivariate patterns in hippocampal subfields under high- and low-curiosity states using an incidental encoding task.
It is well-established that anticipatory and ongoing motivational states influence which experiences are prioritized for memory formation (Düzel et al., 2010; Gruber & Ranganath, 2019; Shohamy & Adcock, 2010). Motivation to learn triggers anticipatory activation in mesolimbic dopaminergic circuits, including the ventral tegmental area (VTA) and the substantia nigra (SN), which modulate hippocampal plasticity to support memory formation (Adcock, Thangavel, Whitfield-Gabrieli, Knutson, & Gabrieli, 2006; Krebs, Heipertz, Schuetze, & Duzel, 2011; Shohamy & Adcock, 2010; Wittmann et al., 2005; Wolosin, Zeithamova, & Preston, 2012). Dopamine plays a key role in the persistence of hippocampal memory traces through a protein-synthesis dependent process known as synaptic tagging and capture (STC) (Frey & Morris, 1997; Navakkode, 2024; Redondo & Morris, 2010). According to the STC hypothesis, weak synaptic activity—such as that occurring during incidental encoding—sets a transient “synaptic tag” at the activated synapses. This tag can capture plasticity-related proteins (PRPs) synthesized in response to strong activation of the same neurons by motivationally salient events (Frey & Morris, 1997; Redondo & Morris, 2010). Dopaminergic input from the VTA to the hippocampus is crucial in this process, as strong VTA activation leads to dopamine release in the hippocampus, which engages D1/D5 receptors and triggers PRP synthesis (Lisman, Grace, & Duzel, 2011; Tsetsenis, Broussard, & Dani, 2023). Importantly, these PRPs can be captured by tagged synapses that were activated in a separate episode within a critical time window, explaining how incidental memories can be strengthened by unrelated motivationally salient experiences. This “spillover” effect may account for the enhanced retention of incidentally encoded information observed when a strong, salient memory is formed in close temporal proximity, as hypothesized to occur during high-curiosity states. Indeed, behavioral studies have demonstrated that novelty, arousal, and reward can enhance memory for incidental information presented either before or after a strong memory trace is formed (Dunsmoor, Murty, Clewett, Phelps, & Davachi, 2022; Lorents, Ruitenberg, & Schomaker, 2023; Quent, Henson, & Greve, 2021; Wang, Tambini, & Lapate, 2022).
Indeed, in a study by Gruber, Gelman, and Ranganath (2014), curiosity enhanced memory for target information as well as temporally proximal irrelevant information, suggesting a sustained encoding state (Fandakova & Gruber, 2020; Galli et al., 2018; Murphy, Dehmelt, Yonelinas, Ranganath, & Gruber, 2021; Padulo et al., 2022; Stare, Gruber, Nadel, Ranganath, & Gómez, 2018). Moreover, Gruber et al. (2014) found that individual differences in activity within the SN/VTA and hippocampus, along with the strength of connectivity between these regions, explained the variability in how well individuals incidentally encoded faces during periods of heightened curiosity. In addition, post-encoding resting state functional connectivity between the hippocampus and dopaminergic midbrain, specifically the VTA is associated with subsequent memory performance (Gruber, Ritchey, Wang, Doss, & Ranganath, 2016; Murty, Tompary, Adcock, & Davachi, 2016; Tompary, Duncan, & Davachi, 2015). Tompary et al. (2015) explored how connectivity between the VTA and distinct subregions of the hippocampus, including CA1, during post-encoding rest relates to long-term memory consolidation. Their findings indicate that stronger connectivity in these regions correlates with enhanced associative memory performance at a 24-hour delay, supporting the hypothesis that midbrain-hippocampal interactions are pivotal for memory consolidation during rest periods (Tambini & Davachi, 2019).
Recent research on multivariate patterns has shown these measures can also effectively predict memory outcomes across various tasks (Brunec, Robin, Olsen, Moscovitch, & Barense, 2020; Favila, Lee, & Kuhl, 2020; Xue, 2018, 2022). Specifically, the similarity of neural patterns between different items encoded within the same period—often referred to as Global Pattern Similarity or Inter-item Pattern Similarity—has been linked to memory performance. Studies have repeatedly shown that items with similar memory outcomes (e.g., remembered vs. forgotten) tend to exhibit greater global neural similarity (Davis, Xue, Love, Preston, & Poldrack, 2014; LaRocque et al., 2013; Lu, Wang, Chen, & Xue, 2015; Uncapher, Boyd-Meredith, Chow, Rissman, & Wagner, 2015; Wagner, Buuren, Bovy, & Fernández, 2016; Ye et al., 2016). This increased similarity is thought to reflect underlying memory strength, the generalization across memories, and the integration of memories with overlapping content (Brunec et al., 2020; Davis et al., 2014).
Importantly, several studies have reported that hippocampal pattern similarity increases between stimuli that share abstract elements or processes, such as attentional states or reward status, and that these increases are correlated with better behavioral performance (Aly & Turk-Browne, 2015; Mack, Love, & Preston, 2016; Wolosin, Zeithamova, & Preston, 2013; Zeithamova, Gelman, Frank, & Preston, 2018). However, the extent to which these effects are driven by the dopaminergic midbrain remains an open question. A study using multivariate pattern analysis (MVPA) found evidence of an anticipatory hippocampal 'convergence state' when participants awaited high- compared to low-value information, which predicted subsequent memory formation (Poh et al., 2022). Crucially, they found that the typicality of anticipatory hippocampal patterns, a measure of how closely a given trial’s pattern of brain activity resembles a prototypical pattern, increased during high curiosity as a function of dopaminergic midbrain activation. However, it remains unclear how dopaminergic activation might create hippocampal states conducive to incidental memory formation at a more granular level, such as at the level of hippocampal subfields.
Rodent models can inform high-resolution neuroimaging analysis of how activation of hippocampal subfields could contribute to curiosity and curiosity-related memory enhancements (Gauthier & Tank, 2018; Hasselmo & Hinman, 2022; McNaughton, 2006; O’Mara, Sanchez-Vives, Brotons-Mas, & O’Hare, 2009a). Among these subfields, the CA1 and subiculum are particularly compelling candidates due to their roles in novelty detection and context/reward integration. The CA1 subfield, which receives inputs from CA3, has been proposed to act as a comparator, detecting mismatches between predicted and actual experiences (Hasselmo & Schnell, 1994; Vinogradova, 2001). This mismatch detection could be a crucial driver of curiosity, as it may signal the need for further exploration and information-seeking to resolve discrepancies (Hasselmo & Hinman, 2022). Findings suggest that VTA inputs preferentially modulate CA1 place fields according to reward contingencies, illustrating how motivation impacts spatial memory encoding (Ghanbarian & Motamedi, 2013; Krishnan, Heer, Cherian, & Sheffield, 2022; Martig & Mizumori, 2011). The subiculum, particularly its ventral region (VSub), plays a significant role in processing context, reward, stress, and anxiety (O’Mara et al., 2009a). The VSub projects to key regions like the lateral septum and amygdala, and it interacts with the ventral tegmental area (VTA) and nucleus accumbens (NAcc) to modulate motivation and reward processing (Andrzejewski, Spencer, & Kelley, 2006; French, Hailstone, & Totterdell, 2003; Herman & Mueller, 2006). Stimulation of the VSub increases dopamine release in the NAcc, prefrontal cortex and VTA, linking it to exploratory behavior (Peleg-Raibstein & Feldon, 2006; Taepavarapruk, Floresco, & Phillips, 2000). Through its strong connections with both CA1 and the subiculum, the VTA forms a critical dopaminergic pathway that integrates reward processing with novelty detection (Lisman et al., 2011).
In this study, we investigated the relationship between hippocampal subfield activation and intrinsic motivation during incidental encoding, using a trivia paradigm commonly employed in curiosity research. We first attempted to replicate previous behavioral findings related to curiosity-enhanced memory and incidental encoding, ensuring that the well-documented effects of curiosity on memory performance were evident in our sample. Building on this, we first analyzed univariate activation differences between high and low curiosity conditions within the hippocampus and dopaminergic midbrain regions, specifically the VTA and SN, to determine whether heightened curiosity is associated with increased activity in these regions that are critical for memory encoding and motivation. Next, we employed multivariate pattern analysis (MVPA) to identify neural correlates of subsequent memory effects related to curiosity, focusing on whether the neural patterns observed during high curiosity states predict better subsequent memory performance, thereby offering insights into the underlying mnemonic processes. Finally, we assessed post-encoding resting state functional connectivity (FC) between VTA and hippocampal subfields, hypothesizing that stronger connectivity within these networks following periods of high curiosity would correlate with enhanced memory consolidation. By leveraging the spatial resolution of ultra-high-field 7T fMRI and insights from animal models, our study aimed to elucidate the roles of specific hippocampal subfields in encoding salient contexts related to intrinsic motivation, thereby bridging the gap between human and animal studies and advancing our understanding of how intrinsic motivation influences memory formation at both the univariate and multivariate levels.