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.
SummaryMammals are able to navigate to hidden goal locations by direct routes that may traverse previously unvisited terrain. Empirical evidence suggests that this “vector navigation” relies on an internal representation of space provided by the hippocampal formation. The periodic spatial firing patterns of grid cells in the hippocampal formation offer a compact combinatorial code for location within large-scale space. Here, we consider the computational problem of how to determine the vector between start and goal locations encoded by the firing of grid cells when this vector may be much longer than the largest grid scale. First, we present an algorithmic solution to the problem, inspired by the Fourier shift theorem. Second, we describe several potential neural network implementations of this solution that combine efficiency of search and biological plausibility. Finally, we discuss the empirical predictions of these implementations and their relationship to the anatomy and electrophysiology of the hippocampal formation.
SummaryThe mammalian hippocampus is important for normal memory function, particularly memory for places and events. Place cells, neurons within the hippocampus that have spatial receptive fields, represent information about an animal’s position. During periods of rest, but also during active task engagement, place cells spontaneously recapitulate past trajectories. Such ‘replay’ has been proposed as a mechanism necessary for a range of neurobiological functions, including systems memory consolidation, recall and spatial working memory, navigational planning, and reinforcement learning. Focusing mainly, but not exclusively, on work conducted in rodents, we describe the methodologies used to analyse replay and review evidence for its putative roles. We identify outstanding questions as well as apparent inconsistencies in existing data, making suggestions as to how these might be resolved. In particular, we find support for the involvement of replay in disparate processes, including the maintenance of hippocampal memories and decision making. We propose that the function of replay changes dynamically according to task demands placed on an organism and its current level of arousal.
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.
Grid cells in the rodent medial entorhinal cortex exhibit remarkably regular spatial firing patterns that tessellate all environments visited by the animal. Two theoretical mechanisms that could generate this spatially periodic activity pattern have been proposed: oscillatory interference and continuous attractor dynamics. Although a variety of evidence has been cited in support of each, some aspects of the two mechanisms are complementary, suggesting that a combined model may best account for experimental data. The oscillatory interference model proposes that the grid pattern is formed from linear interference patterns or "periodic bands" in which velocity-controlled oscillators integrate self-motion to code displacement along preferred directions. However, it also allows the use of symmetric recurrent connectivity between grid cells to provide relative stability and continuous attractor dynamics. Here, we present simulations of this type of hybrid model, demonstrate that it generates intracellular membrane potential profiles that closely match those observed in vivo, addresses several criticisms aimed at pure oscillatory interference and continuous attractor models, and provides testable predictions for future empirical studies.
HighlightsIt is commonly assumed that grid cell inputs generate hippocampal place fields, but recent empirical evidence brings this assumption into doubt.We suggest that place fields are primarily determined by environmental sensory inputs.Grid cells provide a complementary path integration input and large-scale spatial metric.Place and grid cell representations interact to support accurate coding of large-scale space.
Memory retrieval is believed to involve a disparate network of areas, including medial prefrontal and medial temporal cortices, but the mechanisms underlying their coordination remain elusive. One suggestion is that oscillatory coherence mediates inter-regional communication, implicating theta phase and theta-gamma phase-amplitude coupling in mnemonic function across species. To examine this hypothesis, we used non-invasive whole-head magnetoencephalography (MEG) as participants retrieved the location of objects encountered within a virtual environment. We demonstrate that, when participants are cued with the image of an object whose location they must subsequently navigate to, there is a significant increase in 4–8 Hz theta power in medial prefrontal cortex (mPFC), and the phase of this oscillation is coupled both with ongoing theta phase in the medial temporal lobe (MTL) and perceptually induced 65–85 Hz gamma amplitude in medial parietal cortex. These results suggest that theta phase coupling between mPFC and MTL and theta-gamma phase-amplitude coupling between mPFC and neocortical regions may play a role in human spatial memory retrieval. © 2014 The Authors. Hippocampus Published by Wiley Periodicals, Inc.
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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