The hippocampus is crucial for both spatial navigation and episodic memory, suggesting that it provides a common function to both. Here we adapt a spatial paradigm, developed for rodents, for use with functional MRI in humans to show that activation of the right hippocampus predicts the use of an allocentric spatial representation, and activation of the left hippocampus predicts the use of a sequential egocentric representation. Both representations can be identified in hippocampal activity before their effect on behavior at subsequent choice-points. Our results suggest that, rather than providing a single common function, the two hippocampi provide complementary representations for navigation, concerning places on the right and temporal sequences on the left, both of which likely contribute to different aspects of episodic memory.T he hippocampus plays a crucial role in both spatial navigation and episodic memory (1-6). However, the nature of the fundamental hippocampal process or representation that might underlie both functions remains the subject of intense speculation, including suggestions that it is best characterized as associative (7), sequential (8), flexible relational (2), allocentric (1, 5, 9), or spatial contextual (4, 5). Similar speculation surrounds the nature of any lateralization of these representations (1, 5, 10), and whether the firing of hippocampal neurons in freely moving rodents reflects allocentric position, spatial context, or sequential position along a route (5, 11, 12). Here we show that the hippocampus predicts and supports navigation via sequential representations in the left hippocampus and allocentric spatial representations in the right hippocampus. These complementary lateralized representations suggest an explanation for the multiple hippocampal contributions to different aspects of spatial and episodic memory.Within spatial memory a distinction has been made between "allocentric" (world-centered) and "egocentric" (body-centered) representations, with allocentric (or place-learning) and simple egocentric (stimulus response-like) navigation shown to depend on the hippocampus and dorsal striatum, respectively, in rodents (5, 13). recently demonstrated that an additional sequential egocentric representation depends on the rodent hippocampus. The human hippocampus has likewise been associated with allocentric representations of location, allowing accurate navigation from new starting locations (15) based on the configuration of environmental cues (16, 17) or recognition of locations from a new viewpoint (18,19). Similarly, navigation via a fixed route (15, 17) or relative to a single landmark (16), consistent with simple egocentric representations, has been associated with the dorsal striatum. However, to our knowledge, the neural bases of the sequential egocentric representation have not yet been identified in humans, and could provide a link between spatial navigation and episodic memory.Here we adapt the Starmaze task developed for mice (14,20) to investigate the neural base...
At least two main cognitive strategies can be used to solve a complex navigation task: the allocentric or map-based strategy and the sequential egocentric or route-based strategy. The sequential egocentric strategy differs from a succession of independent simple egocentric responses as it requires a sequential ordering of events, possibly sharing functional similarity with episodic memory in this regard. To question the possible simultaneous encoding of sequential egocentric and allocentric strategies, we developed a paradigm in which these two strategies are spontaneously used or imposed. Our results evidenced that sequential egocentric strategy can be spontaneously acquired at the onset of the training as well as allocentric strategy. Allocentric and sequential egocentric strategies could be used together within a trial, and bidirectional shifts (between trials) were spontaneously performed during the training period by 30% of the participants. Regardless of the strategy used spontaneously during the training, all participants could execute immediate shifts to the opposite non previously used strategy when this strategy was imposed. Altogether, our findings suggest that subjects acquire different types of spatial knowledge in parallel, namely knowledge permitting allocentric navigation as well as knowledge permitting sequential egocentric navigation.
To examine the cerebellar contribution to human spatial navigation we used functional magnetic resonance imaging and virtual reality. Our findings show that the sensory-motor requirements of navigation induce activity in cerebellar lobules and cortical areas known to be involved in the motor loop and vestibular processing. By contrast, cognitive aspects of navigation mainly induce activity in a different cerebellar lobule (VIIA Crus I). Our results demonstrate a functional link between cerebellum and hippocampus in humans and identify specific functional circuits linking lobule VIIA Crus I of the cerebellum to medial parietal, medial prefrontal, and hippocampal cortices in nonmotor aspects of navigation. They further suggest that Crus I belongs to 2 nonmotor loops, involved in different strategies: place-based navigation is supported by coherent activity between left cerebellar lobule VIIA Crus I and medial parietal cortex along with right hippocampus activity, while sequence-based navigation is supported by coherent activity between right lobule VIIA Crus I, medial prefrontal cortex, and left hippocampus. These results highlight the prominent role of the human cerebellum in both motor and cognitive aspects of navigation, and specify the cortico-cerebellar circuits by which it acts depending on the requirements of the task.
Episodic memory impairment is a hallmark for early diagnosis of Alzheimer's disease. Most actual tests used to diagnose Alzheimer's disease do not assess the spatiotemporal properties of episodic memory and lead to false-positive or -negative diagnosis. We used a newly developed, nonverbal navigation test for Human, based on the objective experimental testing of a spatiotemporal experience, to differentially Alzheimer's disease at the mild stage (N ϭ 16 patients) from frontotemporal lobar degeneration (N ϭ 11 patients) and normal aging (N ϭ 24 subjects). Comparing navigation parameters and standard neuropsychological tests, temporal order memory appeared to have the highest predictive power for mild Alzheimer's disease diagnosis versus frontotemporal lobar degeneration and normal aging. This test was also nonredundant with classical neuropsychological tests. As a conclusion, our results suggest that temporal order memory tested in a spatial navigation task may provide a selective behavioral marker of Alzheimer's disease.
After making foraging flights of several thousands of kilometres, wandering albatrosses (Diomedea exulans) are able to pinpoint a specific remote island where their nests are located. This impressive navigation ability is highly precise but its nature is mysterious. Here we examined whether albatrosses rely on the perception of the Earth's magnetic field to accomplish this task. We disturbed the perception of the magnetic field using mobile magnets glued to the head of nine albatrosses and compared their performances with those of 11 control birds. We then used satellite telemetry to monitor their behaviour. We found that the ability of birds to home to specific nest sites was unimpaired by this manipulation. In particular, experimental and control birds did not show significant differences with respect to either foraging trip duration, or length, or with respect to homing straightness index. Our data suggest that wandering albatrosses do not require magnetic cues to navigate back to their nesting sites.
Sleep plays a crucial role in the consolidation of newly acquired memories. Yet, how our brain selects the noteworthy information that will be consolidated during sleep remains largely unknown. Here we show that post-learning sleep favors the selectivity of long-term consolidation: when tested three months after initial encoding, the most important (i.e., rewarded, strongly encoded) memories are better retained, and also remembered with higher subjective confidence. Our brain imaging data reveals that the functional interplay between dopaminergic reward regions, the prefrontal cortex and the hippocampus contributes to the integration of rewarded associative memories. We further show that sleep spindles strengthen memory representations based on reward values, suggesting a privileged replay of information yielding positive outcomes. These findings demonstrate that post-learning sleep determines the neural fate of motivationally-relevant memories and promotes a value-based stratification of long-term memory stores.DOI: http://dx.doi.org/10.7554/eLife.07903.001
Abstract. Regular physical exercise has been shown to benefit neurocognitive functions, especially enhancing neurogenesis in the hippocampus. However, the effects of a single exercise session on cognitive functions are controversial. To address this issue, we measured hemodynamic changes in the brain during physical exercise using near-infrared spectroscopy (NIRS) and investigated related effects on memory consolidation processes. Healthy young participants underwent two experimental visits. During each visit, they performed an associative memory task in which they first encoded a series of pictures, then spent 30-min exercising or resting, and finally were asked to recall the picture associations. We used NIRS to track changes in oxygenated hemoglobin concentration over the prefrontal cortex during exercise and rest. To characterize local tissue oxygenation and perfusion, we focused on low frequency oscillations in NIRS, also called vasomotion. We report a significant increase in associative memory consolidation after exercise, as compared to after rest, along with an overall increase in vasomotion. Additionally, performance improvement after exercise correlated positively with power in the neurogenic component (0.02 to 0.04 Hz) and negatively with power in the endothelial component (0.003 to 0.02 Hz). Overall, these results suggest that changes in vasomotion over the prefrontal cortex during exercise may promote memory consolidation processes. © The Authors. Published by SPIE under a Creative Commons Attribution 3.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, including its DOI.
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