Empowering episodic memory through a model-based egocentric navigational training

Psychological Research https://doi.org/10.1007/s00426-022-01777-6 ORIGINAL ARTICLE Empowering episodic memory through a model‑based egocentric navigational training Agustina Fragueiro1 · Annalisa Tosoni1 · Rosalia Di Matteo1 · Giorgia Committeri1 Received: 21 July 2022 / Accepted: 21 November 2022 © The Author(s) 2022 Abstract Recent works have proposed that spatial mechanisms in the hippocampal–entorhinal system might have originally developed to represent distances and positions in the physical space and successively evolved to represent experience and memory in the mental space (Bellmund et al. 2018; Bottini and Doeller 2020). Within this phylogenetic continuity hypothesis (Buzsáki and Moser 2013), mechanisms supporting episodic and semantic memory would have evolved from egocentric and allocentric spatial navigation mechanisms, respectively. Recent studies have described a specific relationship between human performance in egocentric navigation and episodic memory (Committeri et al. 2020; Fragueiro et al. 2021), representing the first behavioral support to this hypothesis. Here, we tested the causal relationship among egocentric navigation and both episodic and semantic components of declarative memory. We conducted two experiments on healthy young adults: in the first experiment, participants were submitted to a navigational training based on path integration, while in the second experiment, participants completed a control training based on visual–perceptual learning. Performance in a set of memory tasks assessing episodic, semantic and short-term memory was compared among the pre- vs. post-training sessions. The results indicated a significant improvement of the episodic memory but not of the semantic or the short-term memory performance following the navigational training. In addition, no modulations of performance across the three memory tasks were observed following the control perceptual training. Our findings provide brand-new evidence of a potential causal association between mechanisms of egocentric navigation and episodic memory, thereby further supporting the phylogenetic continuity hypothesis between navigation and memory mechanisms as well as offering new insights about possible clinical applications of navigational trainings for memory functions/dysfunctions. Keywords Spatial navigation · Declarative memory · Episodic memory · Path integration · Semantic memory Introduction Converging evidence from neuropsychological studies in amnesic patients and spatial navigation research in rats has traditionally indicated a central role of the medial temporal lobe in both declarative memory and spatial navigation functions (Eichenbaum & Cohen, 2014; Epstein et al., 2017). In accordance with this view, a ground-breaking model of hippocampal functions has been recently formulated supporting the idea of a spatial representational format for high-level * Agustina Fragueiro 1 Department of Neuroscience, Imaging and Clinical Sciences, University “G. D’Annunzio”, ITAB, Institute of Advanced Biomedical Technologies, Via Dei Vestini 33, 66100 Chieti, Italy cognition (Bellmund et al., 2018). According to this account, spatial codes associated with neural mapping of positions and distance in the physical environment is also assumed to underlie the mapping and organization of conceptual knowledge and memory in the human cognitive system. Within this view, in particular, processing mechanisms in the hippocampal–entorhinal system are assumed to support knowledge and representation of cognitive space spanned by a set of quality dimensions beyond the Euclidean space for navigation. At a wider evolutionary level, these processing mechanisms in the hippocampal–entorhinal system might have been originally developed to represent distances and positions in the physical space and successively evolved to represent experience and memory in the mental space. Within the phylogenetic continuity hypothesis proposed by Buzsáki and Moser (2013), in particular, high-level mechanisms 13 Vol.:(0123456789) Psychological Research supporting episodic and semantic memory functions would have respectively evolved from egocentric (i.e., self-based) and allocentric (i.e., map-based) spatial navigation mechanisms (see also Bottini & Doeller, 2020, for a review analysis). Within the same model, moreover, map-based/ allocentric navigation would have evolved from self-based/ egocentric navigation, thereby making the basic navigational mechanism of homing the core origin of higher-level functions within both the same domain (navigation) ad across domains (from navigation to memory). Using experimental psychology methods applied to the analysis of human behavior during navigational and memory tasks, we have recently described a statistically specific and predictive relationship between human performance (i.e., accuracy) during egocentric navigation (i.e., path integration performance) and episodic, but not semantic memory tasks (Committeri et al., 2020; Fragueiro et al., 2021). These data represented a first behavioral support to the phylogenetic continuity hypothesis and raised the fascinating possibility that a boosting of the episodic memory abilities could be obtained following a behavioral training in egocentric navigation performance. Accordingly, the implementation of spatial learning strategies engaging the medial temporal lobe has been shown to represent the basis of superior declarative memory functions (Maguire et al., 2003), but to our knowledge, no study has so far addressed the question by employing a basic training on egocentric navigation to indirectly empower episodic memory performance. Of note, as indicated by spatial navigation research in rodents, the hippocampal formation and the afferent structures have been consistently shown to undergo massive forms of synaptic reorganization during prolonged exposure to complex environments and navigation (e.g., Kempermann et al., 1997; van Praag et al., 2000). In the present study, inspired by the phylogenetic continuity model (Buzsáki & Moser, 2013) and the supporting experimental evidence on healthy human performance (Committeri et al., 2020; Fragueiro et al., 2021), we examined the hypothesis of beneficial effects of an egocentric navigational training on episodic memory. To this aim, we conducted a first experiment (Experiment 1) on a group of participants undergoing a proprioceptive path integration training collected in-between a memory evaluation session including an episodic memory task based on film-based temporal order memory, a semantic memory task based on semantic categories and a visual short-term memory task (Fragueiro et al., 2021). The pre- and post-training memory sessions were collected using parallel versions of the same memory tasks, allowing pre- vs. post-training comparisons. A second control experiment (Experiment 2) was conducted on a second group of subjects who performed the same versions of the memory task (...truncated)