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 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.

Mamillary Body Lesions in Monkeys Impair Object-in-Place Memory: Functional Unity of the Fornix-Mamillary System

1997 ◽  
Vol 9 (4) ◽  
pp. 512-521 ◽  
Author(s):  
Amanda Parker ◽  
David Gaffan
Keyword(s):  
Episodic Memory ◽  
Memory Task ◽  
Control Group ◽  
Thalamic Nuclei ◽  
Mamillary Body ◽  
Control Operation ◽  
Place Memory ◽  
Severe Impairment ◽  
Anterior Thalamic Nuclei

Six monkeys were trained preoperatively in an automated object-in-place memory task in which they learned 20 new scenes in each daily session. Three of the six monkeys then received stereotaxically guided bilateral mamillary body lesions, leaving the fornix intact, while the other three received a control operation. Postoperatively the control animals' rate of learning new scenes was unchanged, but the animals with mamillary body lesions showed a severe impairment, equal to that seen in previous experiments after fornix transection. All six animals were then given fornix transection, in addition to the existing mamillary or control operation. The control group now showed, after fornix transection, an impairment equal to that of the animals with mamillary body lesions alone. But the animals with mamillary body lesions did not show any additional impairment following fornix transection. We conclude that (1) the role of the mamillary bodies in a model of human episodic memory is as important as the role of the fornix, (2) the fornix and mamillary bodies form a single functional memory system, since the effect of lesions in both parts is no more severe than the effects of a lesion in one of the parts alone, and (3) the idea that the functional effects of fornix transection result from cholmergic deafferentation of the hippocampus receives no support from the present results; rather, they support the idea that in primates the fornix and mamillary bodies, together with connected structures, including the subiculum, mamillo-thalamic tract, anterior thalamic nuclei, and cingulate bundle, form a cortico-cortical association pathway for episodic memory.

The hippocampus, space, and viewpoints in episodic memory

2002 ◽  
Vol 55 (4) ◽  
pp. 1057-1080 ◽  
Author(s):  
Neil Burgess
Keyword(s):  
Episodic Memory ◽  
Large Scale ◽  
Spatial Information ◽  
Functional Neuroimaging ◽  
Hippocampal Formation ◽  
Spatial Context ◽  
Controlled Study ◽  
Long Term Memory ◽  
Long Term Storage

A computational model of how single neurons in and around the rat hippocampus support spatial navigation is reviewed. The extension of this model, to include the retrieval from human long-term memory of spatial scenes and the spatial context of events is discussed. The model explores the link between spatial and mnemonic functions by supposing that retrieval of spatial information from long-term storage requires the imposition of a particular viewpoint. It is consistent with data relating to representational hemispatial neglect and the involvement of the mammillary bodies, anterior thalamus, and hippocampal formation in supporting both episodic recall and the representation of head direction. Some recent behavioural, neuropsychological, and functional neuroimaging experiments are reviewed, in which virtual reality is used to allow controlled study of navigation and memory for events set within a rich large-scale spatial context. These studies provide convergent evidence that the human hippocampus is involved in both tasks, with some lateralization of function (navigation on the right and episodic memory on the left). A further experiment indicates hippocampal involvement in retrieval of spatial information from a shifted viewpoint. I speculate that the hippocampal role in episodic recollection relates to its ability to represent a viewpoint moving within a spatial framework.

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.

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 Human hippocampal theta power indicates movement onset and distance travelled

2017 ◽  
Vol 114 (46) ◽  
pp. 12297-12302 ◽  
Author(s):  
Daniel Bush ◽  
James A. Bisby ◽  
Chris M. Bird ◽  
Stephanie Gollwitzer ◽  
Roman Rodionov ◽  
...  
Keyword(s):  
Temporal Lobe ◽  
Hippocampal Formation ◽  
Memory Task ◽  
Field Potential ◽  
Sustained Oscillation ◽  
Movement Onset ◽  
Theta Power ◽  
Translational Movement ◽  
Human Hippocampus ◽  
Hippocampal Theta

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 self-paced 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 movement-onset 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.

Spatial View Cells in the Primate Hippocampus: Effects of Removal of View Details

1998 ◽  
Vol 79 (3) ◽  
pp. 1145-1156 ◽  
Author(s):  
Robert G. Robertson ◽  
Edmund T. Rolls ◽  
Pierre Georges-François
Keyword(s):  
Hippocampal Formation ◽  
Memory System ◽  
Parahippocampal Gyrus ◽  
Eye Position ◽  
Hippocampal Function ◽  
Ca1 Region ◽  
Spatial Response ◽  
Representation Of Space ◽  
Spatial View ◽  
Proprioceptive Inputs

Robertson, Robert G., Edmund T. Rolls, and Pierre Georges-François. Spatial view cells in the primate hippocampus: effects of removal of view details. J. Neurophysiol. 79: 1145–1156, 1998. Hippocampal function was analyzed by making recordings from hippocampal formation neurons in macaques actively walking in the laboratory. “Spatial view” cells, which respond when the monkey looks at a part of the environment were analyzed. It is shown that many of these cells retain their spatial characteristics when the view details are obscured totally by curtains and by darkness. It is shown that many of these cells respond more when the monkey is gazing toward one location in the room than toward other locations, even though none of the view details can be seen. Such cells were found in the CA1 region, the parahippocampal gyrus, and the presubiculum. Other cells stopped responding when the monkey looked toward the normally effective location in the environment if the view details were obscured. These cells were in the CA3 region of the hippocampus. The results indicate that for CA3 cells, the visual input is necessary for the normal spatial response of the neurons, and for other cells in the primate hippocampal formation, the response still depends on the monkey gazing toward that location in space when the view details are obscured. These latter cells therefore could reflect the operation of a memory system, in which the neuronal activity can be triggered by factors that probably include not only eye position command/feedback signals, but also probably vestibular and/or proprioceptive inputs. This representation of space “out there” would be an appropriate part of a primate memory system involved in memories of where in an environment an object was seen and more generally in the memory of particular events or episodes for which a spatial component normally provides part of the context.

scholarly journals Reactivated spatial context guides episodic recall

2018 ◽  
Author(s):  
Nora A. Herweg ◽  
Ashwini D. Sharan ◽  
Michael R. Sperling ◽  
Armin Brandt ◽  
Andreas Schulze-Bonhage ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Medial Temporal Lobe ◽  
Spatial Information ◽  
Memory Task ◽  
Spatial Context ◽  
Parahippocampal Gyrus ◽  
Spatial Coding ◽  
Episodic Information ◽  
Neurophysiological Mechanisms ◽  
Hippocampal Theta

AbstractThe medial temporal lobe (MTL) is known as the locus of spatial coding and episodic memory, but the interaction between these cognitive domains, as well as the extent to which they rely on common neurophysiological mechanisms is poorly understood. Here, we use a hybrid spatial-episodic memory task to determine how spatial information is dynamically reactivated in sub-regions of the MTL and how this reactivation guides recall of episodic information. Our results implicate theta oscillations across the MTL as a common neurophysiological substrate for spatial coding in navigation and episodic recall. We further show that spatial context information is initially retrieved in the hippocampus (HC) and subsequently emerges in the parahippocampal gyrus (PHG). Finally, we demonstrate that hippocampal theta phase modulates parahippocampal gamma amplitude during retrieval of spatial context, suggesting a role for cross frequency coupling in coding and transmitting retrieved spatial information.

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 Episodic–like memory in animals: psychological criteria, neural mechanisms and the value of episodic–like tasks to investigate animal models of neurodegenerative disease

2001 ◽  
Vol 356 (1413) ◽  
pp. 1453-1465 ◽  
Author(s):  
Richard G. M. Morris
Keyword(s):  
Episodic Memory ◽  
Neurodegenerative Disease ◽  
Hippocampal Formation ◽  
Amyloid Plaque ◽  
Memory System ◽  
Memory Representation ◽  
Learning Tasks ◽  
The World ◽  
Synaptic Change ◽  
Activity Dependent

The question of whether any non–human species displays episodic memory is controversial. Associative accounts of animal learning recognize that behaviour can change in response to single events but this does not imply that animals need or are later able to recall representations of unique events at a different time and place. The lack of language is also relevant, being the usual medium for communicating about the world, but whether it is critical for the capacity to represent and recall events is a separate matter. One reason for suspecting that certain animals possess an episodic–like memory system is that a variety of learning and memory tasks have been developed that, even though they do not meet the strict criteria required for episodic memory, have an ‘episodic–like’ character. These include certain one–trial learning tasks, scene–specific discrimination learning, multiple reversal learning, delayed matching and non–matching tasks and, most recently, tasks demanding recollection of ‘what, where and when’ an event happened. Another reason is that the neuronal architecture of brain areas thought to be involved in episodic memory (including the hippocampal formation) are substantially similar in mammals and, arguably, all vertebrates. Third, our developing understanding of activity–dependent synaptic plasticity (which is a candidate neuronal mechanism for encoding memory traces) suggests that its expression reflects certain physiological characteristics that are ideal components of a neuronal episodic memory system. These include the apparently digital character of synaptic change at individual terminals and the variable persistence of potentiation accounted for by the synaptic tag hypothesis. A further value of studying episodic–like memory in animals is the opportunity it affords to model certain kinds of neurodegenerative disease that, in humans, affect episodic memory. An example is recent work on a transgenic mouse that over–expresses a mutation of human amyloid precursor protein (APP) that occurs in familial Alzheimer's disease, under the control of platelet derived (PD) growth factor promoter (the PDAPP mouse). A striking age– and amyloid plaque–related deficit is seen using a task in which the mice have to keep changing their memory representation of the world rather than learn a single fact.

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