The anterior medial hippocampus contributes to both recall and familiarity-based memory for scenes

The hippocampus (HC) is a key structure of human behaviour as it has been associated with memory (Squire, 1992), spatial cognition (Moscovitch et al., 2006), language (Duff & Brown-Schmidt, 2012), creative thinking and problem solving (Warren et al., 2016), and decision making (Dickerson et al., 2011). In the domain of memory, the HC is traditionally believed to be responsible for the process of recollection, which involves the rich and contextualised retrieval of an episode (Yonelinas, 2002). In contrast, there has been a longstanding debate regarding the contribution of this structure to familiarity memory, defined as the simple feeling that a stimulus has been encountered before. While some authors have claimed that familiarity is independent of the HC (Eichenbaum et al., 2007), others have argued that this region supports both recollection and familiarity memory (Gold et al., 2006).Table 1.

One influential proposal to resolve this discrepancy is to examine what is retrieved, namely the memory content (Mayes et al., 2007, Saksida and Bussey, 2010). Cumulative evidence showed that the HC is involved in the processing of spatial scenes in memory but also non-memory processes such as future thinking (Addis et al., 2007), imagination (Hassabis et al., 2007, Mullally et al., 2012) and visual perception (Hodgetts et al., 2017, McCormick et al., 2021, Zeidman et al., 2015). This evidence has converged towards the idea that the HC contributes to various domains of cognition through a common mechanism: the construction of spatial scenes (Maguire & Mullally, 2013). In line with this model, we recently showed that the HC is more engaged in recall memory, but also familiarity-based recognition and rejection, for scenes than for objects (Gardette et al., 2022). Importantly, these findings support that the HC can play a role in both recall and familiarity-based memory depending on memory content.

Research have showed that the HC should not be considered as a unitary structure, as internal differences in functional specialisation have been described (Strange et al., 2014). In particular, the sharpness with which information is represented seems to increase gradually along its anterior-posterior axis (Brunec et al., 2018, Poppenk, 2020, Poppenk et al., 2013). More recently, research has also revealed that the HC cortical inputs/outputs vary both along its long and transverse axes (Dalton et al., 2022). Neurons of the posterior-medial HC connect preferentially to visual and other sensory areas, whereas neurons of the anterior-lateral HC are more connected with semantic areas (i.e., inferior lateral temporal cortex). In addition to these gradients of connectivity, Dalton and colleagues showed that the anterior-medial HC (amHC) is particularly connected with temporal, medial parietal, and occipital regions. Crucially, several functional magnetic resonance imaging (fMRI) studies have previously associated amHC activity with various cognitive tasks that imply the construction of a spatial scene (Addis et al., 2012, Dalton et al., 2018, Hodgetts et al., 2017, Lee et al., 2013, Zeidman et al., 2015). These results provide important insights into the functional organization of the HC, and lead to the question of the potential specialisation of different HC sub-regions in memory processes. Because this question was not among our preregistered hypotheses, we did not directly explore whether recall and familiarity-based memory processes were associated with a same or different sub-regions of the HC in our previous study (Gardette et al., 2022). Considering emerging evidence that the amHC plays an important role in scene-based cognition, we hypothesised that this region would be commonly recruited across recall, familiarity-based memory, and visual perception of scene stimuli (i.e., the encoding task). To this end, as was done in previous studies investigating similar questions (e.g., Zeidman et al., 2015), we performed a conjunction analysis between the four tasks performed on scenes and objects. This analysis allowed us to test the hypothesis that a set of brain regions including the amHC was consistently recruited for the processing of scene stimuli, irrespective of the nature of the process engaged (Friston et al., 2005).

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