Recollection is thought to be the hallmark of episodic memory. Here we provide evidence that the hippocampus binds together the diverse elements forming an event, allowing holistic recollection via pattern completion of all elements. Participants learn complex ‘events' from multiple overlapping pairs of elements, and are tested on all pairwise associations. At encoding, element ‘types' (locations, people and objects/animals) produce activation in distinct neocortical regions, while hippocampal activity predicts memory performance for all within-event pairs. When retrieving a pairwise association, neocortical activity corresponding to all event elements is reinstated, including those incidental to the task. Participant's degree of incidental reinstatement correlates with their hippocampal activity. Our results suggest that event elements, represented in distinct neocortical regions, are bound into coherent ‘event engrams' in the hippocampus that enable episodic recollection—the re-experiencing or holistic retrieval of all aspects of an event—via a process of hippocampal pattern completion and neocortical reinstatement.
SummaryGrid cells in the entorhinal cortex (EC) of rodents [1] and humans [2] fire in a hexagonally distributed spatially periodic manner. In concert with other spatial cells in the medial temporal lobe (MTL) [3, 4, 5, 6], they provide a representation of our location within an environment [7, 8] and are specifically thought to allow the represented location to be updated by self-motion [9]. Grid-like signals have been seen throughout the autobiographical memory system [10], suggesting a much more general role in memory [11, 12]. Grid cells may allow us to move our viewpoint in imagination [13], a useful function for goal-directed navigation and planning [12, 14, 15, 16], and episodic future thinking more generally [17, 18]. We used fMRI to provide evidence for similar grid-like signals in human entorhinal cortex during both virtual navigation and imagined navigation of the same paths. We show that this signal is present in periods of active navigation and imagination, with a similar orientation in both and with the specifically 6-fold rotational symmetry characteristic of grid cell firing. We therefore provide the first evidence suggesting that grid cells are utilized during movement of viewpoint within imagery, potentially underpinning our more general ability to mentally traverse possible routes in the service of planning and episodic future thinking.
The formation of associations between items and their context has been proposed to rely on mechanisms distinct from those supporting memory for a single item. Although emotional experiences can profoundly affect memory, our understanding of how it interacts with different aspects of memory remains unclear. We performed three experiments to examine the effects of emotion on memory for items and their associations. By presenting neutral and negative items with background contexts, Experiment 1 demonstrated that item memory was facilitated by emotional affect, whereas memory for an associated context was reduced. In Experiment 2, arousal was manipulated independently of the memoranda, by a threat of shock, whereby encoding trials occurred under conditions of threat or safety. Memory for context was equally impaired by the presence of negative affect, whether induced by threat of shock or a negative item, relative to retrieval of the context of a neutral item in safety. In Experiment 3, participants were presented with neutral and negative items as paired associates, including all combinations of neutral and negative items. The results showed both above effects: compared to a neutral item, memory for the associate of a negative item (a second item here, context in Experiments 1 and 2) is impaired, whereas retrieval of the item itself is enhanced. Our findings suggest that negative affect impairs associative memory while recognition of a negative item is enhanced. They support dual-processing models in which negative affect or stress impairs hippocampal-dependent associative memory while the storage of negative sensory/perceptual representations is spared or even strengthened.
When remembering the past, we typically recall ‘events’ that are bounded in time and space. However, as we navigate our environment our senses receive a continuous stream of information. How do we create discrete long-term episodic memories from continuous input? Although previous research has provided evidence for a role of spatial boundaries in the online segmentation of our sensory experience within working memory, it is not known how this segmentation contributes to subsequent long-term episodic memory. Here we show that the presence of a spatial boundary at encoding (a doorway between two rooms) impairs participants’ later ability to remember the order that objects were presented in. A sequence of two objects presented in the same room in a virtual reality environment is more accurately remembered than a sequence of two objects presented in adjoining rooms. The results are captured by a simple model in which items are associated to a context representation that changes gradually over time, and changes more rapidly when crossing a spatial boundary. We therefore provide the first evidence that the structure of long-term episodic memory is shaped by the presence of a spatial boundary and provide constraints on the nature of the interaction between working memory and long-term memory.
Theta frequency oscillations in the 6-to 10-Hz range dominate the rodent hippocampal local field potential during translational movement, suggesting that theta encodes self-motion. Increases in theta power have also been identified in the human hippocampus during both real and virtual movement but appear as transient bursts in distinct high-and low-frequency bands, and it is not yet clear how these bursts relate to the sustained oscillation observed in rodents. Here, we examine depth electrode recordings from the temporal lobe of 13 presurgical epilepsy patients performing a selfpaced spatial memory task in a virtual environment. In contrast to previous studies, we focus on movement-onset periods that incorporate both initial acceleration and an immediately preceding stationary interval associated with prominent theta oscillations in the rodent hippocampal formation. We demonstrate that movementonset periods are associated with a significant increase in both low (2-5 Hz)-and high (6-9 Hz)-frequency theta power in the human hippocampus. Similar increases in low-and high-frequency theta power are seen across lateral temporal lobe recording sites and persist throughout the remainder of movement in both regions. In addition, we show that movement-related theta power is greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings strengthen the connection between studies of theta-band activity in rodents and humans and offer additional insight into the neural mechanisms of spatial navigation.theta | hippocampus | navigation | spatial memory | intracranial EEG T he rodent hippocampal local field potential (LFP) is dominated by 6-to 10-Hz theta oscillations during translational movement (1, 2). Both the power (1, 3) and frequency (3-6) of theta are positively correlated with running speed. Theta oscillations might therefore encode self-motion information and contribute to the generation of spatially modulated firing patterns (7-9). A critical concern for contemporary neuroscience is to establish whether this hypothesis can be translated across species. During navigation, intracranial recordings from depth electrodes in the human hippocampus have shown that theta is more prevalent during movement than during stationary periods (10-12) and that theta power increases with movement speed (13). In addition, increases in movement-related theta power are seen across the neocortex (10,11,14). These findings support the hypothesis that human theta oscillations might encode self-motion information. However, it has also been demonstrated that human theta-band activity typically occurs in transient bursts distributed throughout movement, in contrast to the continuous high-amplitude oscillation observed in the rodent (15,16). Moreover, these studies identified movement-related oscillations within both higher and lower frequency theta bands (17)(18)(19)(20). Hence, it is not yet clear how theta oscillations in the human hippocampus relate to thos...
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