scholarly journals Time cells in the human hippocampus and entorhinal cortex support episodic memory

2020 ◽  
Author(s):  
Gray Umbach ◽  
Pranish Kantak ◽  
Joshua Jacobs ◽  
Michael Kahana ◽  
Brad E. Pfeiffer ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Entorhinal Cortex ◽  
Cell Activity ◽  
Memory Task ◽  
Temporal Information ◽  
Temporal Organization ◽  
Human Epilepsy ◽  
Human Hippocampus ◽  
Phase Precession ◽  
Episodic Memories

AbstractThe organization of temporal information is critical for the encoding and retrieval of episodic memories. In the rodent hippocampus and entorhinal cortex, recent evidence suggests that temporal information is encoded by a population of “time cells.” We identify time cells in humans using intracranial microelectrode recordings obtained from 27 human epilepsy patients who performed an episodic memory task. We show that time cell activity predicts the temporal organization of episodic memories. A significant portion of these cells exhibits phase precession, a key phenomenon not previously seen in human recordings. These findings establish a cellular mechanism for the representation of temporal information in the human brain needed to form episodic memories.

scholarly journals Time cells in the human hippocampus and entorhinal cortex support episodic memory

2020 ◽  
Vol 117 (45) ◽  
pp. 28463-28474 ◽  
Author(s):  
Gray Umbach ◽  
Pranish Kantak ◽  
Joshua Jacobs ◽  
Michael Kahana ◽  
Brad E. Pfeiffer ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Entorhinal Cortex ◽  
Cell Activity ◽  
Memory Task ◽  
Cellular Mechanism ◽  
Temporal Information ◽  
Temporal Organization ◽  
Human Epilepsy ◽  
Human Hippocampus ◽  
Episodic Memories

The organization of temporal information is critical for the encoding and retrieval of episodic memories. In the rodent hippocampus and entorhinal cortex, evidence accumulated over the last decade suggests that populations of “time cells” in the hippocampus encode temporal information. We identify time cells in humans using intracranial microelectrode recordings obtained from 27 human epilepsy patients who performed an episodic memory task. We show that time cell activity predicts the temporal organization of retrieved memory items. We also uncover evidence of ramping cell activity in humans, which represents a complementary type of temporal information. These findings establish a cellular mechanism for the representation of temporal information in the human brain needed to form episodic memories.

scholarly journals Coding of episodic memory in the human hippocampus

2018 ◽  
Vol 115 (5) ◽  
pp. 1093-1098 ◽  
Author(s):  
John T. Wixted ◽  
Stephen D. Goldinger ◽  
Larry R. Squire ◽  
Joel R. Kuhn ◽  
Megan H. Papesh ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Single Neuron ◽  
Large Fraction ◽  
Memory Task ◽  
Neuron Activity ◽  
Distributed Coding ◽  
Repeated Word ◽  
Human Hippocampus ◽  
Left Hippocampus ◽  
Episodic Memories

Neurocomputational models have long posited that episodic memories in the human hippocampus are represented by sparse, stimulus-specific neural codes. A concomitant proposal is that when sparse-distributed neural assemblies become active, they suppress the activity of competing neurons (neural sharpening). We investigated episodic memory coding in the hippocampus and amygdala by measuring single-neuron responses from 20 epilepsy patients (12 female) undergoing intracranial monitoring while they completed a continuous recognition memory task. In the left hippocampus, the distribution of single-neuron activity indicated that only a small fraction of neurons exhibited strong responding to a given repeated word and that each repeated word elicited strong responding in a different small fraction of neurons. This finding reflects sparse distributed coding. The remaining large fraction of neurons exhibited a concurrent reduction in firing rates relative to novel words. The observed pattern accords with longstanding predictions that have previously received scant support from single-cell recordings from human hippocampus.

scholarly journals Electrical stimulation in hippocampus and entorhinal cortex impairs spatial and temporal memory

2017 ◽  
Author(s):  
Abhinav Goyal ◽  
Jonathan Miller ◽  
Andrew J. Watrous ◽  
Sang Ah Lee ◽  
Tom Coffey ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Entorhinal Cortex ◽  
Temporal Lobe ◽  
Cognitive Processes ◽  
Brain Stimulation ◽  
Medial Temporal Lobe ◽  
Memory Task ◽  
Temporal Organization ◽  
Electrical Brain Stimulation ◽  
Neurosurgical Patients

AbstractThe medial temporal lobe (MTL) is widely implicated in supporting episodic memory and navigation, but its precise functional role in organizing memory across time and space remains elusive. Here we examine the specific cognitive processes implemented by MTL structures (hippocampus and entorhinal cortex) to organize memory by using electrical brain stimulation, leveraging its ability to establish causal links between brain regions and features of behavior. We studied neurosurgical patients of both sexes who performed spatial-navigation and verbal-episodic memory tasks while brain stimulation was applied in various regions during learning. During the verbal memory task, stimulation in the MTL disrupted the temporal organization of encoded memories such that items learned with stimulation tended to be recalled in a more randomized order. During the spatial task, MTL stimulation impaired subjects’ abilities to remember items located far away from boundaries. These stimulation effects were specific to the MTL. Our findings thus provide the first causal demonstration in humans of the specific memory processes that are performed by the MTL to encode when and where events occurred.Significance StatementNumerous studies have implicated the medial temporal lobe (MTL) in encoding spatial and temporal memories, but they have not been able to causally demonstrate the nature of the cognitive processes by which this occurs in real-time. Electrical brain stimulation is able to demonstrate causal links between a brain region and a given function with high temporal precision. By examining behavior in a memory task as subjects received MTL stimulation, we provide the first causal evidence demonstrating the role of the MTL in organizing the spatial and temporal aspects of episodic memory.

scholarly journals Human hippocampal neurons track moments in a sequence of events

2020 ◽  
Author(s):  
Leila Reddy ◽  
Benedikt Zoefel ◽  
Jessy K. Possel ◽  
Judith C. Peters ◽  
Doris Dijksterhuis ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Hippocampal Neurons ◽  
Critical Role ◽  
Memory Task ◽  
Temporal Information ◽  
Firing Activity ◽  
Population Activity ◽  
Sequence Of Events ◽  
Human Hippocampus ◽  
Representation Of Time

AbstractAn indispensable feature of episodic memory is our ability to temporally piece together different elements of an experience into a coherent memory. Hippocampal “time cells” – neurons that represent temporal information – may play a critical role in this process. While these cells have been repeatedly found in rodents, it is still unclear to what extent similar temporal selectivity exists in the human hippocampus. Here we show that temporal context modulates the firing activity of human hippocampal neurons during structured temporal experiences. We recorded neuronal activity in the human brain while patients learned predictable sequences of pictures. We report that human time cells fire at successive moments in this task. Furthermore, time cells also signaled inherently changing temporal contexts during empty 10-second gap periods between trials, while participants waited for the task to resume. Finally, population activity allowed for decoding temporal epoch identity, both during sequence learning and during the gap periods. These findings suggest that human hippocampal neurons could play an essential role in temporally organizing distinct moments of an experience in episodic memory.Significance StatementEpisodic memory refers to our ability to remember the “what, where, and when” of a past experience. Representing time is an important component of this form of memory. Here, we show that neurons in the human hippocampus represent temporal information. This temporal signature was observed both when participants were actively engaged in a memory task, as well as during 10s-long gaps when they were asked to wait before performing the task. Furthermore, the activity of the population of hippocampal cells allowed for decoding one temporal epoch from another. These results suggest a robust representation of time in the human hippocampus.

Object, Space, and Object-Space Representations in the Primate Hippocampus

2005 ◽  
Vol 94 (1) ◽  
pp. 833-844 ◽  
Author(s):  
Edmund T. Rolls ◽  
Jianzhong Xiang ◽  
Leonardo Franco
Keyword(s):  
Episodic Memory ◽  
Spatial Information ◽  
Hippocampal Formation ◽  
Memory Task ◽  
Memory System ◽  
Important Advance ◽  
Object Space ◽  
Place Memory ◽  
Human Hippocampus ◽  
Spatial View

A fundamental question about the function of the primate including human hippocampus is whether object as well as allocentric spatial information is represented. Recordings were made from single hippocampal formation neurons while macaques performed an object-place memory task that required the monkeys to learn associations between objects and where they were shown in a room. Some neurons (10%) responded differently to different objects independently of location; other neurons (13%) responded to the spatial view independently of which object was present at the location; and some neurons (12%) responded to a combination of a particular object and the place where it was shown in the room. These results show that there are separate as well as combined representations of objects and their locations in space in the primate hippocampus. This is a property required in an episodic memory system, for which associations between objects and the places where they are seen are prototypical. The results thus provide an important advance by showing that a requirement for a human episodic memory system, separate and combined neuronal representations of objects and where they are seen “out there” in the environment, is present in the primate hippocampus.

scholarly journals Crucial role for CA2 inputs in the sequential organization of CA1 time cells supporting memory

2021 ◽  
Vol 118 (3) ◽  
pp. e2020698118
Author(s):  
Christopher J. MacDonald ◽  
Susumu Tonegawa
Keyword(s):  
Spatial Working Memory ◽  
Temporal Structure ◽  
Critical Role ◽  
Cell Activity ◽  
Memory Task ◽  
Choice Point ◽  
Temporal Coding ◽  
Temporal Information ◽  
Spatial Coding ◽  
Dorsal Hippocampal

There is considerable evidence for hippocampal time cells that briefly activate in succession to represent the temporal structure of memories. Previous studies have shown that time cells can be disrupted while leaving place cells intact, indicating that spatial and temporal information can be coded in parallel. However, the circuits in which spatial and temporal information are coded have not been clearly identified. Here we investigated temporal and spatial coding by dorsal hippocampal CA1 (dCA1) neurons in mice trained on a classic spatial working-memory task. On each trial, the mice approached the same choice point on a maze but were trained to alternate between traversing one of two distinct spatial routes (spatial coding phase). In between trials, there was a 10-s mnemonic delay during which the mouse continuously ran in a fixed location (temporal coding phase). Using cell-type–specific optogenetic methods, we found that inhibiting dorsal CA2 (dCA2) inputs into dCA1 degraded time cell coding during the mnemonic delay and impaired the mouse’s subsequent memory-guided choice. Conversely, inhibiting dCA2 inputs during the spatial coding phase had a negligible effect on place cell activity in dCA1 and no effect on behavior. Collectively, our work demonstrates that spatial and temporal coding in dCA1 is largely segregated with respect to the dCA2–dCA1 circuit and suggests that CA2 plays a critical role in representing the flow of time in memory within the hippocampal network.

scholarly journals Phase precession in the human hippocampus and entorhinal cortex

2020 ◽  
Author(s):  
Salman E. Qasim ◽  
Itzhak Fried ◽  
Joshua Jacobs
Keyword(s):  
Entorhinal Cortex ◽  
Spatial Information ◽  
Neural Representation ◽  
Local Network ◽  
Neuron Activity ◽  
Human Hippocampus ◽  
Phase Precession ◽  
Show Evidence ◽  
Theta Phase ◽  
Theta Phase Precession

AbstractKnowing where we are, where we have been, and where we are going is critical to many behaviors, including navigation and memory. One potential neuronal mechanism underlying this ability is phase precession, in which spatially tuned neurons represent sequences of positions by activating at progressively earlier phases of local network theta (~5–10 Hz) oscillations. Phase precession may be a general neural pattern for representing sequential events for learning and memory. However, phase precession has never been observed in humans. By recording human single-neuron activity during spatial navigation, we show that spatially tuned neurons in the human hippocampus and entorhinal cortex exhibit phase precession. Furthermore, beyond the neural representation of locations, we show evidence for phase precession related to specific goal-states. Our findings thus extend theta phase precession to humans and suggest that this phenomenon has a broad functional role for the neural representation of both spatial and non-spatial information.

scholarly journals Total recall: episodic memory retrieval, choice, and memory confidence in the rat

2020 ◽  
Author(s):  
Hannah R. Joo ◽  
Hexin Liang ◽  
Jason E Chung ◽  
Charlotte Geaghan-Breiner ◽  
Jiang Lan Fan ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Memory Task ◽  
Correct Choice ◽  
Decision Variable ◽  
Future Behavior ◽  
Episodic Memories ◽  
Past Experiences ◽  
Memory Confidence ◽  
Modern Machine

Episodic memory enables recollection of past experiences to guide future behavior. Humans know which memories to trust (high confidence) and which to doubt (low confidence). How memory retrieval, memory confidence, and memory-guided decisions are related, however, is not understood. Additionally, whether animals can assess confidence in episodic memories to guide behavior is unknown. We developed a spatial episodic memory task in which rats were incentivized to gamble their time: betting more following a correct choice yielded greater reward. Rat behavior reflected memory confidence, with higher temporal bets following correct choices. We applied modern machine learning to identify a memory decision variable, and built a generative model of memories evolving over time that accurately predicted both choices and confidence reports. Our results reveal in rats an ability thought to exist exclusively in primates, and introduce a unified model of memory dynamics, retrieval, choice, and confidence.

scholarly journals Metric and chronological time in human episodic memory

2020 ◽  
Author(s):  
Hallvard Røe Evensmoen ◽  
Lars M. Rimol ◽  
Henning Hoel Rise ◽  
Tor Ivar Hansen ◽  
Hamed Nili ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Time Scales ◽  
Entorhinal Cortex ◽  
Medial Temporal Lobe ◽  
Brain Network ◽  
Parahippocampal Cortex ◽  
Temporal Pole ◽  
Episodic Memories ◽  
Short Time ◽  
Chronological Time

The relative contributions of metric and chronological time in the encoding of episodic memories are unknown. One hundred one healthy young adults viewed 48 unique episodes of visual events and were later tested on recall of the order of events (chronological time) and the precise timing of events (metric time). The behavioral results show that metric recall accuracy correlates with chronological accuracy for events within episodes, but does not play a role on larger time-scales across episodes. Functional magnetic resonance imaging during encoding and recall showed that metric time was represented in the posterior medial entorhinal cortex, as well as the temporal pole and the cerebellum, whereas chronological time was represented in a widespread brain network including the anterior lateral entorhinal cortex, hippocampus, parahippocampal cortex and the prefrontal cortex. We conclude that metric time has a role in episodic memory on short time-scales and is mainly subserved by medial temporal lobe structures.

scholarly journals Episodic memories: how do the hippocampus and the entorhinal ring attractors cooperate to create them?

2020 ◽  
Author(s):  
Krisztián A. Kovács
Keyword(s):  
Episodic Memory ◽  
Entorhinal Cortex ◽  
Clinical Case ◽  
Hippocampal Formation ◽  
New Model ◽  
Spatial Aspect ◽  
Episodic Nature ◽  
Episodic Memories ◽  
The Brain ◽  
Made In

AbstractThe brain is capable of registering a constellation of events, encountered only once, as an episodic memory that can last for a lifetime. As evidenced by the clinical case of the patient HM, memories preserving their episodic nature still depend on the hippocampal formation, several years after being created, while semantic memories are thought to reside in neocortical areas. The neurobiological substrate of one-time learning and life-long storing in the brain, that must exist at the cellular and circuit level, is still undiscovered. The breakthrough is delayed by the fact that studies jointly investigating the rodent hippocampus and entorhinal cortex are mostly targeted at understanding the spatial aspect of learning. Here we present the concept of an entorhinal cortical module, termed EPISODE module, that could explain how the representations of different elements constituting episodic memories can be linked together. The new model that we propose here reconciles the structural and functional observations made in the entorhinal cortex and explains how the downstream hippocampal processing organizes the representations into meaningful sequences.

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