Knowledge

Place cell

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418:. One important aspect of episodic memory is the spatial context in which the event occurred. Hippocampal place cells have stable firing patterns even when cues from a location are removed and specific place fields begin firing when exposed to signals or a subset of signals from a previous location. This suggests that place cells provide the spatial context for a memory by recalling the neural representation of the environment in which the memory occurred. By establishing spatial context, place cells play a role in completing memory patterns. Furthermore, place cells are able to maintain a spatial representation of one location while recalling the neural map of a separate location, effectively differentiating between present experience and past memory. Place cells are therefore considered to demonstrate both pattern completion and pattern separation qualities. 315:
information is any kind of spatial input that might indicate a distance between two points. For example, the edges of an environment might signal the size of the overall place field or the distance between two points within a place field. Metric signals can be either linear or directional. Directional inputs provide information about the orientation of a place field, whereas linear inputs essentially form a representational grid. Contextual cues allow established place fields to adapt to minor changes in the environment, such as a change in object color or shape. Metric and contextual inputs are processed together in the
114: 215:, meaning that they are defined with respect to the outside world rather than the body. By orienting based on the environment rather than the individual, place fields can work effectively as neural maps of the environment. A typical place cell will have only one or a few place fields in a small laboratory environment. However, in larger environments, place cells have been shown to contain multiple place fields which are usually irregular. Place cells may also show directionality, meaning they will only fire in a certain location when travelling in a particular direction. 22: 295: 383: 584:. Place cells have been shown to degenerate in Alzheimer's mouse models, which causes such problems with spatial memory in these mice. Furthermore, the place cells in these models have unstable representations of space, and cannot learn stable representations for new environments as well as place cells in healthy mice. The hippocampal theta waves, as well as the gamma waves, that influence place cell firing, for example through phase precession, are also affected. 154:
designed to provide a subject with spatial information. Recent findings, such as a study showing that place cells respond to non-spatial dimensions, such as sound frequency, disagree with the cognitive map theory. Instead, they support a new theory saying that the hippocampus has a more general function encoding continuous variables, and location just happens to be one of those variables. This fits in with the idea that the hippocampus has a predictive function.
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in color or shape of an object. This suggests that place cells respond to complex stimuli rather than simple individual sensory cues. According to the functional differentation model, sensory information is processed in various cortical structures upstream of the hippocampus before actually reaching the structure, so that the information received by place cells is a compilation, a functional derivative, of different stimuli.
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Contrarily, the CA3 place cells are show increased plasticity in aged subjects. The same place fields in the CA3 region to activate in similar environments, whereas different place fields in young rats would fire in similar environments because they would pick up on subtle differences in these environments. One possible cause of these changes in plasticity may be increased reliance on self-motion cues.
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path, connection between place fields are strengthened due to plasticity, causing subsequent place fields to fire more quickly and causing place field expansion, possibly aiding young rats in spatial memory and learning. However, this observed place field expansion and plasticity is decreased in aged rat subjects, possibly reducing their capacity for spatial learning and memory.
263:. Upon entering a place field, place cells will fire in bursts at a particular point in the phase of the underlying theta waves. However, as an animal progresses through the place field, the firing will happen progressively earlier in the phase. It is thought that this phenomenon increases the accuracy of the place coding, and aids in plasticity, which is required for learning. 120: 506:
are available. Additionally mice can be headfixed, allowing for the use of microscopy techniques to look directly into the brain. Though rats and mice have similar place cells dynamics, mice have smaller place cells, and on the same size track have an increase in number of place fields per cell. Additionally, their replay is weaker compared to the replay in rats.
138:, which also fire only in a particular place, but only when the rat performed an additional behaviour, such as sniffing, which was often correlated with the presence of a novel stimulus, or the absence of an expected stimulus. The findings ultimately supported the cognitive map theory, the idea that the hippocampus hold a spatial representation, a 117: 406:, which are a type of neuron in the entorhinal cortex that relay information to place cells in the hippocampus. Grid cells establish a grid representation of a location, so that during movement place cells can fire according to their new location while orienting according to the reference grid of their external environment. 402:. This is especially the case in the absence of continuous sensory inputs. For example, in an environment with a lack of visuospatial inputs, an animal might search for the environment edge using touch, and discern location based on the distance of its movement from that edge. Path integration is largely aided by 181:. But grid cells may perform a more supporting role in the formation of place fields, such as path integration input. Another non-spatial explanation of hippocampal function suggests that the hippocampus performs clustering of inputs to produce representations of the current context – spatial or non-spatial. 449:, and relay a preliminary representation to form place fields. Place fields are extremely specific, as they are capable of remapping and adjusting firing rates in response to subtle sensory signal changes. This specificity is critical for pattern separation, as it distinguishes memories from one another. 271:
In some cases place cells show directionality, meaning they will only fire in a location when the subject is travelling in a particular direction. However, they may also be omnidirectional, meaning they fire regardless of the direction the subject. The lack of directionality in some place cells might
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remapping. When global remapping occurs, most or all of the place cells remap, meaning they lose or gain a place field, or their place field changes its location. Partial remapping means that most place fields are unchanged and only a small portion of the place cells remap. Some of the changes to the
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There has also been much debate as to whether hippocampal pyramidal cells truly encode non-spatial information as well as spatial information. According to the cognitive map theory, the hippocampus's primary role is to store spatial information through place cells and the hippocampus was biologically
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Both rats and mice are often used as model animals for place cells research. Rats became especially popular after the development of multiarray electrodes, which allows for the simultaneous recording of a large number of cells. However, mice have the advantage that a larger range of genetic variants
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Although place cells primarily rely on visuospatial input, some studies suggest that olfactory input may also affect the formation and stability of place fields. Olfaction may compensate for a loss of visual information, or even be responsible for the formation of stable place fields in the same way
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Remapping refers to the change in the place field characteristics that occurs when a subject experiences a new environment, or the same environment in a new context. This phenomenon was first reported in 1987, and is thought to play a role in the memory function of the hippocampus. There are broadly
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These units were cells that fired in a particular place in the environment, the place field. They are described as having a low resting firing rate (<1 Hz) when a rat is not in its place field, but a particularly high firing rate, which can be over 100 Hz in some cases, within the place
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Place-cell firing patterns are often determined by stimuli in the environment such as visual landmarks, and olfactory and vestibular stimuli. Place cells have the ability to suddenly change their firing pattern from one pattern to another, a phenomenon known as remapping. This remapping may occur in
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is still debated. Spatial view cells respond to locations that are visually explored by eye movement, or the "view of a space", rather than the location of the monkey's body. In the macaque, cells were recorded while the monkey was driving a motorised cab around the experimental room. Additionally,
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for the first time in 2007 by Nachum Ulanovsky and his lab. The place cells in bats have a place field in 3D, which is probably due to the bat flying in three dimensions. The place cells in bats can be based on either vision or echolocation, which remapping taking place when bats switch between the
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Pattern completion is the ability to recall an entire memory from a partial or degraded sensory cue. Place cells are able to maintain a stable firing field even after significant signals are removed from a location, suggesting that they can recall a pattern based on only part of the original input.
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input. An example is the walls of an environment, which provides information about relative distance and location. Place cells generally rely on set distal cues rather than cues in the immediate proximal environment, though local cues can have a profound impact on local place fields. Visual sensory
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Place cells were initially believed to fire in direct relation to simple sensory inputs, but studies have suggested that this may not be the case. Place fields are usually unaffected by large sensory changes, like removing a landmark from an environment, but respond to subtle changes, like a change
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in the environment, on environmental boundaries, or on an interaction between the two. Additionally, not all place cells rely on the same external cues. One important distinction in cues is local and distal, where local cues appear in the immediate vicinity of a subject, whereas distal cues are far
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region remains the same between young and aged rats, average firing rate in this region is higher in aged rats. Young rats exhibit place field plasticity: when they are moving along a straight path, place fields are activated one after another. When young rats repeatedly traverse the same straight
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is one such environment where directionality does occur. In this environment, cells may even have multiple place fields, of which one is strongly directional, while the others are not. In virtual reality corridors, the degree of directionality in the population of place cells is particularly high.
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Place cells often exhibit reactivation outside their place fields. This reactivation has a much faster time scale than the actual experience, and it occurs mostly in the same order in which it was originally experienced, or, more rarely, in reverse. Replay is believed to have a functional role in
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Aged rats further show a high instability in their place cells in the CA1 region. When introduced to the same environment several times, the hippocampal map of the environment changed about 30% of the time, suggesting that the place cells are remapping in response to the exact same environment.
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Furthermore, the pattern completion exhibited by place cells is symmetric, because an entire memory can be retrieved from any part of it. For example, in an object-place association memory, spatial context can be used to recall an object and the object can be used to recall the spatial context.
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Sensory information received by place cells can be categorized as either metric or contextual information, where metric information corresponds to where place cells should fire and contextual input corresponds to whether or not a place field should fire in a certain environment. Metric sensory
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Place cells were first discovered by John O'Keefe and Jonathan Dostrovsky in 1971 in rats' hippocampuses. They noticed that rats with impairments in their hippocampus performed poorly in spatial tasks, and thus hypothesised that this area must hold some kind of spatial representation of the
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of sensory neurons, in that the firing region corresponds to a region of sensory information in the environment. However, unlike receptive fields, place cells show no topography, meaning that two neighboring cells do not necessarily have neighboring place fields. Place cells fire spikes in
177:, pyramidal cells in the entorhinal cortex. This theory suggests that the place fields of the place cells are a combination of several grid cells, which have hexagonal grid-like patterns of activity. The theory has been supported by computational models. The relation may arise through 472:. However, when replay is disturbed, it does not necessarily affect place coding, which means it is not essentially for consolidation in all circumstances. The same sequence of activity may occur before the actual experience. This phenomenon, termed preplay, may have a role in 277:
The directionality of place cells has been shown to emerge as a result of the animal's behaviour. For example, the receptive fields become skewed when rats travel a linear track in a single direction. Recent theoretical studies suggest that place cells encode a
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Place field properties, including the rate of firing and spike characteristics such as width and amplitude of the spikes, are largely similar between young and aged rats in the CA1 hippocampal region. However, while the size of place fields in the hippocampal
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information. A change in color of a specific object or the walls of the environment can affect whether or not a place cell fires in a particular field. Thus, visuospatial sensory information is critical to the formation and recollection of place field.
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Place cells were first discovered in rats, but place cells and place-like cells have since been found in a number of different animals, including rodents, bats and primates. Additionally, evidence for place cells in humans was found in 2003.
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away, and act more like landmarks. Individual place cells have been shown to follow either or rely on both. Additionally, the cues on which the place cells rely may depend on previous experience of the subject and the saliency of the cue.
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Hori, Etsuro; Nishio, Yoichi; Kazui, Kenichi; Umeno, Katsumi; Tabuchi, Eiichi; Sasaki, Kazuo; Endo, Shunro; Ono, Taketoshi; Nishijo, Hisao (2005). "Place-related neural responses in the monkey hippocampal formation in a virtual space".
69:– the reactivation of the place cells involved in a certain experience at a much faster timescale. Place cells show alterations with age and disease, such as Alzheimer's disease, which may be involved in a decrease of memory function. 29:
layer of a rat. The rat ran back and forth along an elevated track, stopping at each end to eat a small food reward. Dots indicate positions where action potentials were recorded, with color indicating which neuron emitted that action
54:. Place cells work with other types of neurons in the hippocampus and surrounding regions to perform this kind of spatial processing. They have been found in a variety of animals, including rodents, bats, monkeys and humans. 281:
which maps the current state to the predicted successor states, and that directionality emerges from this formalism. This computational framework also provides an account for the distortion of place fields around obstacles.
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in the hippocampus. They noted that some of the cells showed activity when a rat was "situated in a particular part of the testing platform facing in a particular direction". These cells would later be called place cells.
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Bourboulou, Romain; Marti, Geoffrey; Michon, François-Xavier; El Feghaly, Elissa; Nouguier, Morgane; Robbe, David; Koenig, Julie; Epsztein, Jerome (2019-03-01). Burgess, Neil; Behrens, Timothy E; Burke, Sara N (eds.).
362:, such as rotations, can cause changes in place cells firing. After receiving vestibular input some place cells may remap to align with this input, though not all cells will remap and are more reliant on visual cues. 350:
visuospatial cues are. This has been confirmed by a study in a virtual environment that was composed of odor gradients. Change in the olfactory stimulus in an environment may also cause the remapping of place cells.
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environment that have been shown to induce remapping include changing the shape or size of the environment, the color of the walls, the smell in the environment, or the relevance of a location to the task at hand.
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Mably, Alexandra J.; Gereke, Brian J.; Jones, Dylan T.; Colgin, Laura Lee (2017). "Impairments in spatial representations and rhythmic coordination of place cells in the 3xTg mouse model of Alzheimer's disease".
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Place cell firing rate decreases dramatically after ethanol exposure, causing reduced spatial sensitivity, which has been hypothesised to be the cause of impairments in spatial procession after alcohol exposure.
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place-related responses have been found macaques while they navigated in a virtual reality. More recently, place cells may have been identified in the hippocampus of freely moving macaques and marmosets.
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This video shows a rat running around in a circular environment (black line) and any time a particular cell is active (red dots). The red dots cluster around one location, which is the place field of the
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Ekstrom, Arne D.; Kahana, Michael J.; Caplan, Jeremy B.; Fields, Tony A.; Isham, Eve A.; Newman, Ehren L.; Fried, Itzhak (2003-09-11). "Cellular networks underlying human spatial navigation".
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McNaughton, B. L.; Barnes, C. A.; O'Keefe, J. (1983-09-01). "The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats".
617:, exhibit decreased activity in aged subjects. The application of memantine leads to in increase in place field plasticity in aged rat subjects. Although memantine aids in the 2957:
Smith, Paul F.; Darlington, Cynthia L.; Zheng, Yiwen (29 April 2009). "Move it or lose itβ€”Is stimulation of the vestibular system necessary for normal spatial memory?".
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Geva-Sagiv, Maya; Las, Liora; Yovel, Yossi; Ulanovsky, Nachum (2015). "Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation".
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Geva-Sagiv, Maya; Las, Liora; Yovel, Yossi; Ulanovsky, Nachum (2015). "Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation".
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Movement can also be an important spatial cue. Mice use their self-motion information to determine how far and in which direction they have travelled, a process called
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lesions of the vestibular system in patients may cause abnormal firing of hippocampal place cells as evidenced, in part, by difficulties with spatial tasks such as the
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An example of place cell remapping, with the location of the place field of cell 1 changing between environment, and cell 2 losing its place field in environment 2.
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Save, Etienne; Ludek Nerad; Bruno Poucet (23 February 2000). "Contribution of multiple sensory information to place field stability in hippocampal place cells".
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Wiener, S. I.; Korshunov, V. A.; Garcia, R.; Berthoz, A. (1995-11-01). "Inertial, substratal and landmark cue control of hippocampal CA1 place cell activity".
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Behrens, Timothy E. J.; Muller, Timothy H.; Whittington, James C. R.; Mark, Shirley; Baram, Alon B.; Stachenfeld, Kimberly L.; Kurth-Nelson, Zeb (2018-10-24).
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which is known to improve spatial memory, and was therefore used in an attempt to restore place field plasticity in aged subjects. NMDA receptors, which are
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Jeffery, Kathryn; Michael Anderson; Robin Hayman; Subhojit Chakraborty (2004). "A proposed architecture for the neural representation of spatial context".
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Delpolyi, AR; Rankin, K; Mucke, L; Miller, BL; Gorno-Tempini, ML (4 September 2007). "Spatial cognition and the human navigation network in AD and MCI".
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Geva-Sagiv, Maya; Romani, Sandro; Las, Liora; Ulanovsky, Nachum (2016). "Hippocampal global remapping for different sensory modalities in flying bats".
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inputs are examples of sensory inputs that are utilized by place cells. These types of sensory cues can include both metric and contextual information.
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Hazama, Yutaro; Tamura, Ryoi (2019-05-14). "Effects of self-locomotion on the activity of place cells in the hippocampus of a freely behaving monkey".
4882:"Impairments in experience-dependent scaling and stability of hippocampal place fields limit spatial learning in a mouse model of Alzheimer's disease" 5046: 858:
O'Keefe, J.; Dostrovsky, J. (November 1971). "The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat".
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Courellis, Hristos S.; Nummela, Samuel U.; Metke, Michael; Diehl, Geoffrey W.; Bussell, Robert; Cauwenberghs, Gert; Miller, Cory T. (2019-12-09).
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Leutgeb, Stefan; Leutgeb, Jill K; Moser, May-Britt; Moser, Edvard I (2005-12-01). "Place cells, spatial maps and the population code for memory".
445:, a section of the hippocampus involved in memory formation and retrieval. Granule cells in the dentate gyrus process sensory information using 58:
either some of the place cells or in all place cells at once. It may be caused by a number of changes, such as in the odor of the environment.
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Muir, Gary M.; Brown, Joel E.; Carey, John P.; Hirvonen, Timo P.; Santina, Charles C. Della; Minor, Lloyd B.; Taube, Jeffrey S. (2009-11-18).
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Ono, Taketoshi; Nakamura, Kiyomi; Fukuda, Masaji; Tamura, Ryoi (1991-01-02). "Place recognition responses of neurons in monkey hippocampus".
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two. Bats also have social place cells; this finding was published in Science at the same time as the report of social place cells in rats.
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White, Aaron M.; Matthews, Douglas B.; Best, Phillip J. (2000). "Ethanol, memory, and hippocampal function: A review of recent findings".
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Nakazawa, Kazu; Thomas McHugh; Matthew Wilson; Susumu Tonegawa (May 2004). "NMDA Receptors, Place Cells and Hippocampal Spatial Memory".
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Moser, Edvard I.; Kropff, Emilio; Moser, May-Britt (2008). "Place Cells, Grid Cells, and the Brain's Spatial Representation System".
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Bostock, Elizabeth; Muller, Robert U.; Kubie, John L. (1991). "Experience-dependent modifications of hippocampal place cell firing".
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Yartsev, Michael M.; Ulanovsky, Nachum (2013-04-19). "Representation of Three-Dimensional Space in the Hippocampus of Flying Bats".
2737: 1386: 65:. They contain information about the spatial context a memory took place in. And they seem to perform consolidation by exhibiting 3737:
Las, Liora; Ulanovsky, Nachum (2014), Derdikman, Dori; Knierim, James J. (eds.), "Hippocampal Neurophysiology Across Species",
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Poucet, Bruno; Save, Etienne; Lenck-Santini, Pierre-Pascal (2011). "Sensory and Memory Properties of Hippocampal Place Cells".
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at a high frequency inside the place field, but outside of the place field they remain relatively inactive. Place fields are
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Ulanovsky, Nachum; Moss, Cynthia F. (2007). "Hippocampal cellular and network activity in freely moving echolocating bats".
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process of spatial information in aged rat subjects, it does not help with the retrieval of this information later in time.
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Pattern separation is the ability to differentiate one memory from other stored memories. Pattern separation begins in the
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Place cells fire in a specific region of an environment, known as a place field. Place fields are roughly analogous to the
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occur particularly in impoverished environments, whereas in more complicated environments directionality is enhanced. The
4018:"Disruption of the Head Direction Cell Signal after Occlusion of the Semicircular Canals in the Freely Moving Chinchilla" 50:. Place cells are thought to act collectively as a cognitive representation of a specific location in space, known as a 1373:
O'Keefe, John (3 September 1999). "Do hippocampal pyramidal cells signal non-spatial as well as spatial information?".
1143:"Dynamic Interactions between Local Surface Cues, Distal Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells" 678: 516:
Rats furthermore have social place cells, cells which encode the position of other rats. This finding was published in
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Lew, Adena R. (7 February 2011). "Looking beyond the boundaries: Time to put landmarks back on the cognitive map?".
696:"Instability in the Place Field Location of Hippocampal Place Cells after Lesions Centered on the Perirhinal Cortex" 594: 77: 4236: 310:(DG) and the different hippocampal subfields (CA1 and CA3). Inset shows the wiring between these different areas. 2618:
Jeffery, Kathryn (5 July 2007). "Integration of the Sensory Inputs to Place Cells: What, Where, Why, and How?".
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O'Keefe, J; Recce, M. L. (1993). "Phase relationship between hippocampal place units and the EEG theta rhythm".
26: 4760:"Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model" 5084: 5068: 1488: 371: 4452:
Rolls, Edmund T. (1999). "Spatial view cells and the representation of place in the primate hippocampus".
3902:"Comparing Mouse and Rat Hippocampal Place Cell Activities and Firing Sequences in the Same Environments" 5094: 2573:"Local remapping of place cell firing in the Tolman detour task: Place cell firing and detour behavior" 46:
that becomes active when an animal enters a particular place in its environment, which is known as the
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Wilson, M. A.; McNaughton, B. L. (1993-08-20). "Dynamics of the hippocampal ensemble code for space".
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Smith, David; Sheri Mizumori (10 June 2006). "Hippocampal Place Cells, Context, and Episodic Memory".
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Jeffery, Kathryn (2007). "Integration of Sensory Inputs to Place Cells: what, where, why, and how?".
102: 3791: 3132: 2094:"The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells" 1212: 805: 3003:
Jacob, Pierre-Yves; Poucet, Bruno; Liberge, Martine; Save, Etienne; Sargolini, Francesca (2014).
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Zhao, Rong; Fowler, Stephanie W.; Chiang, Angie C. A.; Ji, Daoyun; Jankowsky, Joanna L. (2014).
4429:"Researchers identify 'social place cells' in the brain that respond to the locations of others" 3961:"Functional imaging of hippocampal place cells at cellular resolution during virtual navigation" 3959:
Dombeck, Daniel A.; Harvey, Christopher D.; Tian, Lin; Looger, Loren L.; Tank, David W. (2010).
2475:"Functional imaging of hippocampal place cells at cellular resolution during virtual navigation" 2473:
Dombeck, Daniel A.; Harvey, Christopher D.; Tian, Lin; Looger, Loren L.; Tank, David W. (2010).
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Eichenbaum, Howard; Dudchenko, Paul; Wood, Emma; Shapiro, Matthew; Tanila, Heikki (1999-06-01).
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Place cells are found in the hippocampus, a structure in the medial temporal lobe of the brain.
1653:"A non-spatial account of place and grid cells based on clustering models of concept learning" 5040: 1088: 787: 299: 129:
In 1976, O'Keefe performed a follow-up study, demonstrating the presence of what they called
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Cacucci, Francesca; Yi, Ming; Wills, Thomas J.; Chapman, Paul; O'Keefe, John (2008-06-03).
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Spatial cues such as geometric boundaries or orienting landmarks are important examples of
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O'Keefe, John (1976-01-01). "Place units in the hippocampus of the freely moving rat".
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There has been much debate as to whether hippocampal place cells function depends on
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O'Keefe, John; Nadel, Lynn (1 December 1979). "The Hippocampus as a Cognitive Map".
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of distance and direction travelled from a start point to estimate current position.
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In addition to rats and mice, place cells have also been found in
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Place-activated hippocampus cells found in some mammals
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Place cells are thought to play an important role in
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4318: 4314: 4259: 4255: 4246: 4244: 4233: 4226: 4179: 4175: 4128: 4124: 4071: 4067: 4014: 4010: 3977:10.1038/nn.2648 3957: 3953: 3898: 3891: 3836: 3832: 3792:10.1.1.408.4443 3767: 3763: 3757: 3735: 3718: 3670: 3663: 3632:10.1038/nrn3888 3616: 3612: 3557: 3553: 3508: 3504: 3443: 3439: 3400:(12): 744–757. 3386: 3382: 3337:Current Biology 3329: 3325: 3278: 3271: 3224: 3213: 3190:10.1038/nrn1385 3174: 3165: 3133:10.1.1.141.1450 3116: 3107: 3060: 3056: 3001: 2994: 2955: 2948: 2895: 2891: 2854:Cerebral Cortex 2846: 2842: 2835: 2819: 2812: 2775:(2–3): 95–112. 2765: 2761: 2722: 2715: 2659: 2655: 2616: 2612: 2569: 2565: 2528: 2524: 2491:10.1038/nn.2648 2471: 2467: 2414: 2407: 2354: 2347: 2308: 2299: 2262: 2258: 2205: 2194: 2139: 2135: 2090: 2083: 2030: 2023: 1976: 1972: 1925: 1921: 1890:10.1038/nrn3888 1874: 1870: 1831: 1818: 1763: 1759: 1714: 1710: 1649: 1645: 1592: 1588: 1543: 1539: 1508:10.1038/nn.4650 1491: 1485: 1478: 1417: 1410: 1371: 1362: 1323: 1304: 1257: 1253: 1213:10.1.1.463.1315 1196: 1192: 1139: 1135: 1104: 1100: 1061: 1057: 1004: 1000: 953: 944: 928:10.1038/514153a 899: 895: 856: 849: 839: 837: 833: 827: 823: 814: 812: 804: 803: 799: 752: 737: 692: 688: 681: 667: 663: 659: 631: 590: 574: 565: 560: 547:common marmoset 539: 526: 503: 486: 461: 455: 439: 433: 424: 416:episodic memory 412: 410:Episodic memory 380: 378:Movement inputs 368:radial arm maze 356: 347: 329: 298:Anatomy of the 288: 274:radial arm maze 269: 253: 247: 229: 200: 195: 171: 113: 107:extracellularly 98: 86:May-Britt Moser 76:was awarded to 63:episodic memory 17: 12: 11: 5: 5108: 5098: 5097: 5092: 5087: 5073: 5072: 5058: 5057:External links 5055: 5053: 5052: 4980: 4929: 4892:(8): 963–978. 4872: 4837:(4): 378–392. 4817: 4750: 4707: 4656: 4597: 4546: 4511:(1): 194–198. 4495: 4460:(4): 467–480. 4444: 4420: 4363: 4328:(7): 952–958. 4312: 4253: 4224: 4195:10.1038/nn1829 4189:(2): 224–233. 4173: 4122: 4065: 4008: 3951: 3889: 3830: 3761: 3755: 3716: 3681:(8): 991–996. 3661: 3610: 3551: 3502: 3437: 3380: 3343:(1): R37–R50. 3323: 3288:(6): 738–746. 3269: 3211: 3184:(5): 368–369. 3163: 3126:(9): 716–729. 3105: 3054: 2992: 2946: 2889: 2860:(2): 423–432. 2840: 2833: 2810: 2759: 2713: 2653: 2626:(9): 775–785. 2610: 2563: 2542:(3): 707–715. 2522: 2465: 2405: 2368:(5): 734–744. 2345: 2297: 2276:(3): 221–227. 2256: 2192: 2133: 2104:(7): 1951–68. 2081: 2044:(9): 469–477. 2021: 1970: 1935:(4): 419–439. 1919: 1868: 1841:(2): 201–218. 1816: 1777:(1): 343–350. 1757: 1708: 1643: 1606:(3): 136–145. 1586: 1557:(2): 490–509. 1537: 1476: 1408: 1381:(4): 352–364. 1360: 1302: 1267:(2): 193–205. 1251: 1206:(2): 180–192. 1190: 1133: 1114:(3): 484–507. 1098: 1071:(4): 487–533. 1055: 1018:(2): 209–226. 998: 942: 893: 866:(1): 171–175. 860:Brain Research 847: 821: 810:Nobelprize.org 797: 762:(9): 775–785. 735: 686: 680:978-0198572060 679: 660: 658: 655: 654: 653: 648: 643: 638: 630: 627: 611:NMDA receptors 589: 586: 578:spatial memory 576:Problems with 573: 570: 564: 561: 559: 556: 538: 535: 525: 522: 502: 499: 485: 482: 457:Main article: 454: 451: 432: 429: 423: 420: 411: 408: 379: 376: 355: 352: 346: 343: 328: 325: 287: 284: 268: 267:Directionality 265: 249:Main article: 246: 243: 236:remapping and 228: 225: 199: 196: 194: 191: 170: 167: 136:misplace units 97: 94: 15: 9: 6: 4: 3: 2: 5107: 5096: 5093: 5091: 5088: 5086: 5083: 5082: 5080: 5070: 5065: 5061: 5060: 5048: 5042: 5034: 5030: 5025: 5020: 5015: 5010: 5006: 5002: 4998: 4991: 4989: 4987: 4985: 4976: 4972: 4968: 4964: 4960: 4956: 4952: 4948: 4944: 4940: 4933: 4925: 4921: 4916: 4911: 4907: 4903: 4899: 4895: 4891: 4887: 4883: 4876: 4868: 4864: 4860: 4856: 4852: 4848: 4844: 4840: 4836: 4832: 4824: 4822: 4813: 4809: 4804: 4799: 4795: 4791: 4786: 4781: 4777: 4773: 4769: 4765: 4761: 4754: 4746: 4742: 4738: 4734: 4730: 4726: 4722: 4718: 4711: 4703: 4699: 4695: 4691: 4687: 4683: 4679: 4675: 4671: 4667: 4660: 4652: 4648: 4643: 4638: 4634: 4630: 4625: 4620: 4616: 4612: 4608: 4601: 4593: 4589: 4585: 4581: 4577: 4573: 4569: 4565: 4561: 4557: 4550: 4542: 4538: 4534: 4530: 4526: 4522: 4518: 4514: 4510: 4506: 4499: 4491: 4487: 4483: 4479: 4475: 4471: 4467: 4463: 4459: 4455: 4448: 4434: 4430: 4424: 4416: 4412: 4408: 4404: 4399: 4394: 4390: 4386: 4382: 4378: 4374: 4367: 4359: 4355: 4351: 4347: 4343: 4339: 4335: 4331: 4327: 4323: 4316: 4308: 4304: 4300: 4296: 4292: 4288: 4284: 4280: 4276: 4272: 4268: 4264: 4257: 4242: 4238: 4231: 4229: 4220: 4216: 4212: 4208: 4204: 4200: 4196: 4192: 4188: 4184: 4177: 4169: 4165: 4161: 4157: 4153: 4149: 4145: 4141: 4137: 4133: 4126: 4118: 4114: 4110: 4106: 4101: 4096: 4092: 4088: 4084: 4080: 4076: 4069: 4061: 4057: 4052: 4047: 4043: 4039: 4035: 4031: 4027: 4023: 4019: 4012: 4004: 4000: 3995: 3990: 3986: 3982: 3978: 3974: 3970: 3966: 3962: 3955: 3947: 3943: 3938: 3933: 3929: 3925: 3920: 3915: 3911: 3907: 3903: 3896: 3894: 3885: 3881: 3877: 3873: 3869: 3865: 3861: 3857: 3853: 3849: 3845: 3841: 3834: 3826: 3822: 3818: 3814: 3810: 3806: 3802: 3798: 3793: 3788: 3784: 3780: 3776: 3772: 3765: 3758: 3752: 3748: 3744: 3740: 3733: 3731: 3729: 3727: 3725: 3723: 3721: 3712: 3708: 3704: 3700: 3696: 3692: 3688: 3684: 3680: 3676: 3668: 3666: 3657: 3653: 3649: 3645: 3641: 3637: 3633: 3629: 3626:(2): 94–108. 3625: 3621: 3614: 3606: 3602: 3597: 3592: 3588: 3584: 3579: 3574: 3570: 3566: 3562: 3555: 3547: 3543: 3539: 3535: 3530: 3525: 3521: 3517: 3513: 3506: 3498: 3494: 3489: 3484: 3480: 3476: 3472: 3468: 3464: 3460: 3456: 3452: 3448: 3441: 3433: 3429: 3424: 3419: 3415: 3411: 3407: 3403: 3399: 3395: 3391: 3384: 3376: 3372: 3367: 3362: 3358: 3354: 3350: 3346: 3342: 3338: 3334: 3327: 3319: 3315: 3311: 3307: 3303: 3299: 3295: 3291: 3287: 3283: 3276: 3274: 3265: 3261: 3256: 3251: 3246: 3241: 3237: 3233: 3229: 3222: 3220: 3218: 3216: 3207: 3203: 3199: 3195: 3191: 3187: 3183: 3179: 3172: 3170: 3168: 3159: 3155: 3151: 3147: 3143: 3139: 3134: 3129: 3125: 3121: 3114: 3112: 3110: 3101: 3097: 3093: 3089: 3085: 3081: 3077: 3073: 3069: 3065: 3058: 3050: 3046: 3041: 3036: 3032: 3028: 3023: 3018: 3014: 3010: 3006: 2999: 2997: 2988: 2984: 2980: 2976: 2972: 2968: 2964: 2960: 2953: 2951: 2942: 2938: 2933: 2928: 2924: 2920: 2916: 2912: 2908: 2904: 2900: 2893: 2885: 2881: 2876: 2871: 2867: 2863: 2859: 2855: 2851: 2844: 2836: 2830: 2826: 2825: 2817: 2815: 2806: 2802: 2798: 2794: 2790: 2786: 2782: 2778: 2774: 2770: 2763: 2755: 2751: 2747: 2743: 2739: 2735: 2731: 2727: 2720: 2718: 2709: 2705: 2700: 2695: 2691: 2687: 2682: 2677: 2673: 2669: 2665: 2657: 2649: 2645: 2641: 2637: 2633: 2629: 2625: 2621: 2614: 2606: 2602: 2598: 2594: 2590: 2586: 2582: 2578: 2574: 2567: 2559: 2555: 2550: 2545: 2541: 2537: 2533: 2526: 2518: 2514: 2509: 2504: 2500: 2496: 2492: 2488: 2484: 2480: 2476: 2469: 2461: 2457: 2452: 2447: 2443: 2439: 2435: 2431: 2427: 2423: 2419: 2412: 2410: 2401: 2397: 2392: 2387: 2383: 2379: 2375: 2371: 2367: 2363: 2359: 2352: 2350: 2341: 2337: 2333: 2329: 2325: 2321: 2318:(3): 317–30. 2317: 2313: 2306: 2304: 2302: 2293: 2289: 2284: 2279: 2275: 2271: 2270:Psychobiology 2267: 2260: 2252: 2248: 2243: 2238: 2234: 2230: 2226: 2222: 2218: 2214: 2210: 2203: 2201: 2199: 2197: 2188: 2184: 2179: 2174: 2170: 2166: 2161: 2156: 2152: 2148: 2144: 2137: 2129: 2125: 2120: 2115: 2111: 2107: 2103: 2099: 2095: 2088: 2086: 2077: 2073: 2069: 2065: 2061: 2057: 2052: 2047: 2043: 2039: 2035: 2028: 2026: 2017: 2013: 2009: 2005: 2001: 1997: 1993: 1989: 1985: 1981: 1974: 1966: 1962: 1958: 1954: 1950: 1946: 1942: 1938: 1934: 1930: 1923: 1915: 1911: 1907: 1903: 1899: 1895: 1891: 1887: 1884:(2): 94–108. 1883: 1879: 1872: 1864: 1860: 1856: 1852: 1848: 1844: 1840: 1836: 1829: 1827: 1825: 1823: 1821: 1812: 1808: 1803: 1798: 1793: 1788: 1784: 1780: 1776: 1772: 1768: 1761: 1753: 1749: 1744: 1739: 1735: 1731: 1727: 1723: 1719: 1712: 1704: 1700: 1695: 1690: 1686: 1682: 1678: 1674: 1670: 1666: 1662: 1658: 1654: 1647: 1639: 1635: 1630: 1625: 1621: 1617: 1613: 1609: 1605: 1601: 1597: 1590: 1582: 1578: 1574: 1570: 1565: 1560: 1556: 1552: 1548: 1541: 1533: 1529: 1525: 1521: 1517: 1513: 1509: 1505: 1501: 1497: 1490: 1483: 1481: 1472: 1468: 1463: 1458: 1454: 1450: 1446: 1442: 1438: 1434: 1430: 1426: 1422: 1415: 1413: 1404: 1400: 1396: 1392: 1388: 1384: 1380: 1376: 1369: 1367: 1365: 1356: 1352: 1348: 1344: 1340: 1336: 1332: 1328: 1321: 1319: 1317: 1315: 1313: 1311: 1309: 1307: 1298: 1294: 1290: 1286: 1282: 1278: 1274: 1270: 1266: 1262: 1255: 1247: 1243: 1239: 1235: 1231: 1227: 1223: 1219: 1214: 1209: 1205: 1201: 1194: 1186: 1182: 1177: 1172: 1168: 1164: 1160: 1156: 1152: 1148: 1144: 1137: 1129: 1125: 1121: 1117: 1113: 1109: 1102: 1094: 1090: 1086: 1082: 1078: 1074: 1070: 1066: 1059: 1051: 1047: 1043: 1039: 1035: 1031: 1026: 1021: 1017: 1013: 1009: 1002: 994: 990: 986: 982: 978: 974: 970: 966: 963:(1): 78–109. 962: 958: 951: 949: 947: 938: 934: 929: 924: 920: 916: 913:(7521): 153. 912: 908: 904: 897: 889: 885: 881: 877: 873: 869: 865: 861: 854: 852: 832: 825: 811: 807: 801: 793: 789: 785: 781: 777: 773: 769: 765: 761: 757: 750: 748: 746: 744: 742: 740: 731: 727: 722: 717: 713: 709: 705: 701: 697: 690: 682: 676: 672: 665: 661: 652: 649: 647: 644: 642: 639: 636: 633: 632: 626: 622: 620: 616: 612: 608: 604: 599: 596: 585: 583: 579: 569: 555: 552: 548: 544: 534: 531: 521: 519: 514: 512: 507: 494: 490: 484:Model animals 481: 479: 475: 471: 467: 460: 450: 448: 444: 443:dentate gyrus 438: 428: 419: 417: 407: 405: 401: 393: 389: 384: 375: 373: 369: 365: 361: 351: 342: 339: 334: 324: 322: 318: 309: 308:dentate gyrus 305: 301: 296: 292: 286:Sensory input 283: 280: 275: 264: 262: 258: 252: 242: 239: 235: 220: 216: 214: 210: 205: 186: 182: 180: 176: 163: 159: 155: 151: 148: 143: 141: 140:cognitive map 137: 132: 111: 108: 104: 93: 91: 87: 83: 79: 75: 70: 68: 64: 59: 55: 53: 52:cognitive map 49: 45: 41: 38:is a kind of 37: 28: 23: 19: 5041:cite journal 5004: 5000: 4945:(1): 30–40. 4942: 4938: 4932: 4889: 4885: 4875: 4834: 4830: 4767: 4763: 4753: 4720: 4716: 4710: 4672:(1): 88–93. 4669: 4665: 4659: 4614: 4611:PLOS Biology 4610: 4600: 4559: 4555: 4549: 4508: 4504: 4498: 4457: 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30:potential. 4959:1471-0048 4906:1098-1063 4851:1098-1063 4794:0027-8424 4717:Neurology 4686:1098-1063 4633:1545-7885 4576:0304-3940 4562:: 32–37. 4525:0304-3940 4474:1098-1063 4407:0036-8075 4342:1546-1726 4291:0036-8075 4203:1546-1726 4152:1471-0048 4109:0036-8075 4042:0270-6474 3985:1546-1726 3928:1662-5102 3868:0036-8075 3809:1476-4687 3787:CiteSeerX 3695:1098-1063 3640:1471-0048 3587:2090-5904 3479:0028-0836 3414:1471-0048 3357:0960-9822 3302:0959-4388 3128:CiteSeerX 3084:0953-816X 3031:1662-5145 2789:2191-0200 2690:2050-084X 2499:1546-1726 2442:0270-6474 2382:0959-4388 2292:0889-6313 2233:0270-6474 2169:1662-5153 2060:0166-2236 2000:1432-1106 1949:0301-0082 1898:1471-0048 1685:2041-1723 1620:0166-2236 1573:0896-6273 1532:205441266 1516:1546-1726 1453:0028-0836 1281:1098-1063 1230:1098-1063 1208:CiteSeerX 1167:0270-6474 1093:616519952 1085:144038992 1034:0896-6273 977:0014-4886 880:0006-8993 792:621877128 603:memantine 364:Bilateral 321:olfactory 227:Remapping 147:landmarks 72:The 2014 5033:20802800 4967:16371948 4924:24752989 4859:28032686 4812:18505838 4745:23800745 4737:17785667 4702:12921247 4694:10706220 4651:31815940 4592:72332794 4584:30738872 4541:27398046 4482:10495028 4433:phys.org 4415:29326274 4358:23242606 4350:27239936 4307:21953971 4299:23599496 4211:17220886 4160:29386614 4117:29326273 4060:19923286 4003:20890294 3946:30297987 3884:15611758 3817:12968182 3711:35411577 3703:16108028 3656:18397443 3648:25601780 3605:21918724 3546:52092903 3538:30146305 3497:21179088 3432:30356103 3375:29316421 3310:16263261 3264:24198767 3198:15100719 3150:16897724 3100:10675209 3049:24926239 2987:10344864 2979:19405142 2941:29483530 2884:24008582 2797:10718148 2754:34908637 2746:10706218 2708:30822270 2640:17615579 2605:41211033 2597:21395871 2558:10774737 2517:20890294 2400:21820895 2251:14523083 2187:29354038 2076:17019065 2068:18687478 1914:18397443 1906:25601780 1863:36456584 1855:15172764 1703:31831749 1638:24485517 1581:30359611 1524:28967910 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Index


CA1
pyramidal neuron
hippocampus
place field
cognitive map
episodic memory
replay
Nobel Prize in Physiology or Medicine
John O'Keefe
Edvard
May-Britt Moser
grid cells
chronic electrode implants
extracellularly
cognitive map
landmarks

Grid cells
grid cells
Hebbian learning

receptive fields
bursts
allocentric

Phase precession
theta waves
phase precession
radial arm maze

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