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 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 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 tasks before and after a visual–perceptual training. We predicted a specific, causal effect of the navigational training on episodic memory performance but not semantic or short-term memory performance. Furthermore, we expected an improvement of the episodic memory performance following the egocentric navigation but not the perceptual control training.
Discussion
Based on our previous findings of a specific and predictive relationship between self-based human abilities in path integration and temporal order memory tasks (Committeri et al.,
2020; Fragueiro et al.,
2021), here we tested whether a causal relationship could be described between human processing of egocentric spatial navigation and episodic memory. This question was originally raised from a pivotal work by Buzsáki and Moser on the neurophysiologically derived model of a phylogenetic continuity between mechanisms of navigation in the physical and mental space (memory) (Buzsáki & Moser,
2013). According to this model, in particular, the organizational principles underlying declarative memory would have inherited the fundamental distinction between the spatial reference systems (self-based vs. map-based), supporting navigation in the physical world. Within this view, therefore, episodic memory functions would have evolved from egocentric/self-based navigation and semantic memory functions from allocentric/map-based navigation.
In accordance with this model, and in particular with the egocentric navigation/episodic memory edge of the model predictions, the present results indicated a significant improvement of the episodic memory but not of the semantic or short-term memory performance following an egocentric navigational training. In contrast, no modulations of performance were observed in any of the three memory tasks following a perceptual training on visual discrimination of target shapes. These results suggest that the observed empowerment of the episodic memory performance following the navigational training was associated with the specific properties of the egocentric training and not solely explained by unspecific modulatory effects of task repetition and/or cognitive training. These findings, therefore, provide a general support to the phylogenetic continuity hypothesis between mechanisms of spatial navigation and memory.
In humans, few recent studies have reported improvements in declarative memory performance following a navigational training. A single case study on a patient suffering from topographical disorientation, for example, has described a secondary positive effect of an imagery-based navigational training on episodic memory (Boccia et al.,
2019). At the group level, instead, an improvement of long-term memory capabilities (recognition memory) has been observed in older individuals following a training program on a wayfinding game in virtual reality (Wais et al,
2021). In this study, an immersive, complex environment was employed, in which, as for navigational rodent model studies, participants were requested to navigate in novel and unfamiliar surroundings to complete assigned errands and wayfinding. In this case, advancement in performance was probably based on efficient transformation of navigational strategies and environmental representations from egocentric (route-based) to allocentric (survey-based).
Differently from these studies, here we showed a specific modulation of the episodic memory performance following an egocentric navigational training and we speculate that the observed effect might be explained by a core processing similarity between the episodic memory task based on temporal order memory for complex audio–visual material (i.e., movies) and the path integration task based on a continuous spatial updating of both angular displacement and distance from a reference point within an environment (Loomis et al.,
1999).
Accordingly, Buzsáki and Moser (
2013) have proposed that the mechanisms for representing a path through an environment are basically the same for representing episodes in memory, and the capacity of the brain to generate and store sequences seems to be the key mechanism supporting both self-based navigation and episodic memory. More specifically, as the position-dependent sequential firing of neurons along a linear path, sequences linking arbitrary items in episodic memory are essentially unidimensional. At the neurophysiological level, this shared mechanism for generating neural sequences would be supported by theta phase-modulation of gamma power in the hippocampus and entorhinal cortex (Buzsáki and Moser,
2013; Colgin et al.,
2009). Within this view, therefore, the continuous spatial updating of the self-position over time during path integration might represent the basic spatial code for the temporal processing of episodes/events. In this respect, it is worth noticing that the proprioceptive path integration training employed in our study was based on a continuous updating of the self-position from proprioceptive/idiothetic and vestibular information, which might be assumed to reinforce the spatial awareness of the body movement in space, and then provide a refined self-based reference system during subsequent temporal order memory judgments. As far as the specific type of navigational training, finally, we might not exclude that also other forms of egocentric navigational training, such as couplings between a recognition point and the direction in which the route continues, might induce a modulation of the episodic memory performance but we argue that the sequential updating aspect of the path integration training might represent the core mechanism supporting the observed modulation on the memory performance.
The findings presented in the current study suggest a possible booster effect of proprioceptive path integration training on temporal order memory for episodic details. These findings not only further support the model of a phylogenetic continuity between egocentric navigation and episodic memory functions but also provide new insights for possible clinical applications of the egocentric navigational training in the field of memory deficits. We suggest, in particular, that individuals with episodic memory deficits might benefit from an egocentric navigational training for the empowerment and possibly recovery of episodic memory abilities. In line with this hypothesis, deficits in self-based navigation abilities, also specifically involving the path integration performance, have been reported in healthy aging (Allen et al.,
2004; Skolimowska et al.,
2011; Xie et al.,
2017), mild cognitive impairment and Alzheimer’s disease (Mokrisova et al.,
2016). Deficits in path integration abilities have been previously associated with compromised entorhinal grid cell computations (Stangl et al.,
2018), and both path integration and grid cells deficits have been proposed as sensitive biomarkers of pathological decline in early Alzheimer’s disease (Bierbrauer et al.,
2020; Howett et al.,
2019; Kunz et al.,
2015; Segen et al.,
2022). Egocentric heading based on path integration, moreover, has also been thought to more closely support the clinical discrimination between Alzheimer’s and non-Alzheimer’s dementia than navigational tasks based on allocentric, map-based knowledge (Tu et al.,
2017). Future research might test the potential effects of a self-based navigational training on older adults and patients with memory deficits. Within this context, it is worth mentioning that, compared to young adults, task performance in healthy elderly people has been thought to more heavily rely on visual processing components rather than on bodily (i.e., tactile, kinematic, proprioceptive) factors, leading to the conclusion that older adults are less embodied than young adults (Costello & Bloesch,
2017). Within this framework, we speculate that a proprioceptive path integration training might also provide a clinical tool for minimizing age-related deficits in multimodal integration and embodied cognition in addition to memory functions.
As far as possible limitations of our study, we acknowledge that the episodic memory task was slightly more difficult than the semantic and short-term memory tasks. However, all three memory tasks were specifically developed with a medium–high difficulty level to avoid roof effects and, therefore, training-induced modulations of performance could be potentially observed for any of the three tasks. Accordingly, a modulation of performance in the post- vs. the pre-training session was also observed for the semantic memory task, but the analyses indicated no statistical significance of the effect. Moreover, the lack of a statistically significant three-way interaction in the mixed-model ANOVA imposes caution on conclusions about a strong causal-specific effect of the navigational vs. the perceptual training. On this basis, therefore, we acknowledge that our results can be more properly thought of as an initial and preliminary, rather than a definitive evidence of a beneficial effect of an egocentric navigational training on episodic memory performance, which could be exploited for potential applications in the clinical field. At a more theoretical level, finally, we acknowledge that our study specifically focuses on the egocentric navigation/episodic memory edge of the phylogenetic continuity model proposed by Buszáki and Moser (2013) and no definitive knowledge has been acquired so far about the association and causal relationship between allocentric/map-based navigation and semantic memory functions. Future studies, therefore, will hopefully conduct specific examinations on this point as well as on possible higher-order interactions between the 4 model components.
In conclusion, the present data offer the first causal evidence for the hypothesis of a phylogenetic continuity between spatial navigation and declarative memory, showing that navigation through time in mental space shares core processing mechanisms with egocentric navigation in the physical space. At the same time, the data offer a new perspective toward clinical applications because training the core, egocentric/self-based navigation through path integration could potentially have boosting effects on episodic, temporally-based memory in both physiological and pathological aging.
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