429:. 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.
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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
226:, 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.
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595:. 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.
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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.
274:. 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.
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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.
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149:, 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
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417:, 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.
413:. 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
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192:. 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.
460:, 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.
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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
188:, 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
483:. 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
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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".
80:– 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.
40:
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
65:. 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.
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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.
2672:
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.).
373:, 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.
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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.
135:
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".
1989:
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".
628:, 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
661:
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Smith, Paul F.; Darlington, Cynthia L.; Zheng, Yiwen (29 April 2009). "Move it or lose it—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.
4565:
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".
4893:"Impairments in experience-dependent scaling and stability of hippocampal place fields limit spatial learning in a mouse model of Alzheimer's disease"
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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".
456:, a section of the hippocampus involved in memory formation and retrieval. Granule cells in the dentate gyrus process sensory information using
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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".
689:
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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".
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76:. They contain information about the spatial context a memory took place in. And they seem to perform consolidation by exhibiting
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88:
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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
4029:"Disruption of the Head Direction Cell Signal after Occlusion of the Semicircular Canals in the Freely Moving Chinchilla"
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61:. Place cells are thought to act collectively as a cognitive representation of a specific location in space, known as a
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O'Keefe, John (3 September 1999). "Do hippocampal pyramidal cells signal non-spatial as well as spatial information?".
1154:"Dynamic Interactions between Local Surface Cues, Distal Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells"
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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?".
707:"Instability in the Place Field Location of Hippocampal Place Cells after Lesions Centered on the Perirhinal Cortex"
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321:(DG) and the different hippocampal subfields (CA1 and CA3). Inset shows the wiring between these different areas.
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2629:
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".
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4771:"Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model"
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Rolls, Edmund T. (1999). "Spatial view cells and the representation of place in the primate hippocampus".
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3913:"Comparing Mouse and Rat Hippocampal Place Cell Activities and Firing Sequences in the Same Environments"
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2584:"Local remapping of place cell firing in the Tolman detour task: Place cell firing and detour behavior"
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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?".
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2105:"The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells"
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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).
4440:"Researchers identify 'social place cells' in the brain that respond to the locations of others"
3972:"Functional imaging of hippocampal place cells at cellular resolution during virtual navigation"
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Dombeck, Daniel A.; Harvey, Christopher D.; Tian, Lin; Looger, Loren L.; Tank, David W. (2010).
2486:"Functional imaging of hippocampal place cells at cellular resolution during virtual navigation"
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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.
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331:
271:
261:
4769:
Cacucci, Francesca; Yi, Ming; Wills, Thomas J.; Chapman, Paul; O'Keefe, John (2008-06-03).
3401:"The hippocampal sharp wave–ripple in memory retrieval for immediate use and consolidation"
1349:
342:
Spatial cues such as geometric boundaries or orienting landmarks are important examples of
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284:
214:
96:
73:
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3015:
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1639:
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1186:
1169:
1153:
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O'Keefe, John (1976-01-01). "Place units in the hippocampus of the freely moving rat".
731:
722:
706:
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5089:
4527:
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1951:
1812:
1777:
1542:
1095:
979:
882:
621:
453:
447:
318:
156:
There has been much debate as to whether hippocampal place cells function depends on
150:
117:
62:
4755:
4712:
4602:
4551:
4368:
4317:
3894:
3721:
3666:
3556:
3110:
2997:
2861:"Spatial Olfactory Learning Contributes to Place Field Formation in the Hippocampus"
2791:
2764:
2615:
2086:
1924:
1873:
1857:
1365:
1307:
1074:
O'Keefe, John; Nadel, Lynn (1 December 1979). "The Hippocampus as a Cognitive Map".
405:
of distance and direction travelled from a start point to estimate current position.
4985:
4877:
4500:
4229:
4178:
4044:
3835:
3328:
3216:
2815:
2658:
2350:
2026:
1975:
1413:
1256:
1060:
1019:"The Hippocampus, Memory, and Place Cells: Is It Spatial Memory or a Memory Space?"
1003:
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229:
92:
4948:
Burke, Sara N.; Barnes, Carol A. (2006). "Neural plasticity in the ageing brain".
3168:
4634:
4578:
3757:
3539:
3522:
3239:"The mechanisms for pattern completion and pattern separation in the hippocampus"
1574:
1557:
1103:
802:
54:
3304:
2933:
2675:"Dynamic control of hippocampal spatial coding resolution by local visual cues"
2384:
2061:
2044:
1727:
O'Keefe, J; Burgess, N; Donnett, J. G.; Jeffery, K. J.; Maguire, E. A. (1998).
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Etienne, Ariane S.; Jeffery, Kathryn J. (2004). "Path integration in mammals".
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521:
484:
267:
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4643:
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4535:
4484:
4417:
4382:
Omer, David B.; Maimon, Shir R.; Las, Liora; Ulanovsky, Nachum (2018-01-12).
4352:
4301:
4213:
4162:
4119:
4052:
3995:
3938:
3929:
3911:
Mou, Xiang; Cheng, Jingheng; Yu, Yan S. W.; Kee, Sara E.; Ji, Daoyun (2018).
3878:
3819:
3705:
3650:
3597:
3489:
3424:
3367:
3312:
3255:
3094:
3041:
3032:
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2700:
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2452:
2392:
2302:
2243:
2179:
2170:
2152:
Latuske, Patrick; Kornienko, Olga; Kohler, Laura; Allen, Kevin (2018-01-04).
2070:
2010:
1959:
1908:
1695:
1630:
1583:
1526:
1498:
Stachenfeld, Kimberly L.; Botvinick, Matthew M.; Gershman, Samuel J. (2017).
1463:
1291:
1240:
1177:
1044:
987:
890:
4795:
4408:
4383:
4293:
4110:
4085:
3870:
2876:
842:"Scientific Background: The Brain's Navigational Place and Grid Cell System"
651:
613:
414:
185:
172:
100:
5043:
4977:
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4170:
4127:
4070:
4013:
3956:
3827:
3713:
3658:
3615:
3548:
3507:
3458:"Preplay of future place cell sequences by hippocampal cellular assemblies"
3442:
3385:
3320:
3274:
3208:
3160:
3059:
2989:
2951:
2894:
2807:
2756:
2718:
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2527:
2410:
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1534:
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1405:
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1138:
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947:
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740:
17:
5074:
4543:
3886:
3588:
3102:
2470:
2342:
2138:
2018:
1821:
1802:
1762:
1432:"Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit"
1299:
995:
898:
145:
field. Additionally, O'Keefe described six special cells, which he called
5008:"Neural protein synthesis during aging: effects on plasticity and memory"
3523:"Generative Predictive Codes by Multiplexed Hippocampal Neuronal Tuplets"
1967:
488:
219:
157:
4154:
3811:
3481:
3016:"Vestibular control of entorhinal cortex activity in spatial navigation"
2691:
2275:
Deadwyler, Sam A.; Breese, Charles R.; Hampson, Robert E. (1989-09-01).
1455:
195:
4908:
4853:
4689:
10.1002/(SICI)1098-1063(2000)10:1<88::AID-HIPO10>3.0.CO;2-L
4477:
10.1002/(SICI)1098-1063(1999)9:4<467::AID-HIPO13>3.0.CO;2-F
3697:
3152:
2981:
2642:
2543:"Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields"
2293:
2276:
2002:
1938:
O'Keefe, John (1979-01-01). "A review of the hippocampal place cells".
1232:
778:
2749:
10.1002/(SICI)1098-1063(2000)10:1<64::AID-HIPO7>3.0.CO;2-Y
2541:
Mehta, Mayank R.; Quirk, Michael C.; Wilson, Matthew A. (March 2000).
1733:
Philosophical Transactions of the Royal Society B: Biological Sciences
1398:
10.1002/(SICI)1098-1063(1999)9:4<352::AID-HIPO3>3.0.CO;2-1
2220:"Heterogeneous Modulation of Place Cell Firing by Changes in Context"
1558:"What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior"
1130:
175:
and place cells work together to determine the position of the animal
4961:
4344:
3987:
3642:
3200:
2501:
2043:
Colgin, Laura Lee; Moser, Edvard I.; Moser, May-Britt (2008-09-01).
1900:
1518:
938:
913:
4205:
4084:
Danjo, Teruko; Toyoizumi, Taro; Fujisawa, Shigeyoshi (2018-01-12).
3342:Ólafsdóttir, H. Freyja; Bush, Daniel; Barry, Caswell (2018-01-08).
3572:"Reactivation, Replay, and Preplay: How It Might All Fit Together"
520:
In addition to rats and mice, place cells have also been found in
502:
392:
304:
228:
194:
168:
167:
123:
31:
2429:"On the directional firing properties of hippocampal place cells"
591:
and navigation are thought to be one of the early indications of
4618:"Spatial encoding in primate hippocampus during free navigation"
116:, with which they could record the activity of individual cells
3521:
Liu, Kefei; Sibille, Jeremie; Dragoi, George (September 2018).
2427:
Muller, R. U.; Bostock, E.; Taube, J. S.; Kubie, J. L. (1994).
1729:"Place cells, navigational accuracy, and the human hippocampus"
36:
Spatial firing patterns of eight place cells recorded from the
4086:"Spatial representations of self and other in the hippocampus"
531:
at the same time as the report of social place cells in bats.
330:
before reaching the hippocampal place cells. Visuospatial and
1430:
Aronov, Dmitriy; Nevers, Rhino; Tank, David W. (2017-03-29).
2369:"Models of Place and Grid Cell Firing and Theta Rhythmicity"
1776:
Bures J, Fenton AA, Kaminsky Y, Zinyuk L (7 January 1997).
612:
This plasticity can be rescued in aged rats by giving them
5006:
Schimanski, Lesley, A.; Barnes, Carol A. (6 August 2010).
2582:
Alvernhe, Alice; Save, Etienne; Poucet, Bruno (May 2011).
1605:
Bush, Daniel; Barry, Caswell; Burgess, Neil (2014-03-01).
184:
It has been proposed that place cells are derivatives of
2859:
Zhang, Sijie; Denise Manahan-Vaughn (5 September 2013).
2218:
Anderson, Michael I.; Jeffery, Kathryn J. (2003-10-01).
552:
Place-related responses have been found in cells of the
266:
The firing of place cells is timed in relation to local
4141:
Bray, Natasha (2018). "An 'other' kind of place cell".
3344:"The Role of Hippocampal Replay in Memory and Planning"
2963:
2961:
1839:
1837:
1835:
1833:
1831:
27:
Place-activated hippocampus cells found in some mammals
4834:
4832:
3124:
3122:
3120:
1607:"What do grid cells contribute to place cell firing?"
112:
environment. To test this hypothesis, they developed
72:
Place cells are thought to play an important role in
3678:
3676:
2908:
Radvansky, Brad; Daniel Dombeck (26 February 2018).
2045:"Understanding memory through hippocampal remapping"
3750:
Space, Time and Memory in the Hippocampal Formation
662:
List of distinct cell types in the adult human body
648:, primate hippocampal counterpart for visual field.
5001:
4999:
4997:
4995:
3570:Buhry, Laure; Azizi, Amir H.; Cheng, Sen (2011).
3456:Dragoi, George; Tonegawa, Susumu (January 2011).
2277:"Control of place-cell activity in an open field"
2154:"Hippocampal Remapping and Its Entorhinal Origin"
914:"Nobel prize for decoding brain's sense of place"
760:
758:
756:
754:
752:
750:
560:, however, whether these are true place cells or
3232:
3230:
3228:
3226:
817:"The Nobel Prize in Physiology or Medicine 2014"
4775:Proceedings of the National Academy of Sciences
1782:Proceedings of the National Academy of Sciences
1662:Mok, Robert M.; Love, Bradley C. (2019-12-12).
2910:"An olfactory virtual reality system for mice"
3295:. Motor systems / Neurobiology of behaviour.
2367:Burgess, Neil; O’Keefe, John (October 2011).
2316:
2314:
2312:
1379:
1377:
1375:
912:Abbott, Alison; Callaway, Ewen (2014-10-09).
8:
5056:: CS1 maint: multiple names: authors list (
4384:"Social place-cells in the bat hippocampus"
2730:
2728:
705:Muir, Gary; David K. Bilkey (1 June 2001).
5033:
5023:
4924:
4812:
4794:
4651:
4633:
4407:
4109:
4060:
4003:
3946:
3928:
3801:
3605:
3587:
3538:
3497:
3432:
3375:
3264:
3254:
3142:
3049:
3031:
2941:
2884:
2708:
2690:
2558:
2517:
2460:
2400:
2292:
2251:
2187:
2169:
2128:
2060:
1811:
1801:
1752:
1703:
1638:
1573:
1471:
1222:
1185:
1034:
937:
730:
91:for the discovery of place cells, and to
3399:Joo, Hannah R.; Frank, Loren M. (2018).
1846:Neuroscience & Biobehavioral Reviews
672:
5049:
4248:"The Bat Man: Neuroscience on the Fly"
4241:
4239:
3906:
3904:
3743:
3741:
3739:
3737:
3735:
3733:
3731:
3286:
3284:
3182:
3180:
3178:
3009:
3007:
2827:
2825:
1493:
1491:
1350:10.1146/annurev.neuro.31.061307.090723
425:Place cells play an important role in
3752:, Springer Vienna, pp. 431–461,
3020:Frontiers in Integrative Neuroscience
2835:The Neurobiology of Spatial Behaviour
2422:
2420:
2362:
2360:
2213:
2211:
2209:
2207:
2098:
2096:
2038:
2036:
1500:"The hippocampus as a predictive map"
1425:
1423:
1331:
1329:
1327:
1325:
1323:
1321:
1319:
1317:
85:Nobel Prize in Physiology or Medicine
7:
3075:The European Journal of Neuroscience
2158:Frontiers in Behavioral Neuroscience
2103:Muller, R. U.; Kubie, J. L. (1987).
961:
959:
957:
864:
862:
840:Kiehn, Ole; Forssberg, Hans (2014).
569:Disturbances to place cell function
397:Grid and place cells contribute to
4740:10.1212/01.wnl.0000271376.19515.c6
3917:Frontiers in Cellular Neuroscience
3087:10.1111/j.1460-9568.1995.tb00642.x
2445:10.1523/JNEUROSCI.14-12-07235.1994
2236:10.1523/JNEUROSCI.23-26-08827.2003
2121:10.1523/JNEUROSCI.07-07-01951.1987
1778:"Place cells and place navigation"
1170:10.1523/JNEUROSCI.22-14-06254.2002
723:10.1523/JNEUROSCI.21-11-04016.2001
682:The Hippocampus as a Cognitive Map
25:
4246:Abbott, Alison (September 2018).
3243:Frontiers in Systems Neuroscience
507:A rat with an electrode implanted
464:Reactivation, replay, and preplay
347:inputs can also supply important
58:
5073:
2600:10.1111/j.1460-9568.2011.07653.x
2588:European Journal of Neuroscience
1152:Knierim, James J. (2002-07-15).
5012:Frontiers in Aging Neuroscience
3293:Current Opinion in Neurobiology
2792:10.1515/REVNEURO.2000.11.2-3.95
2373:Current Opinion in Neurobiology
1858:10.1016/j.neubiorev.2003.12.002
4045:10.1523/JNEUROSCI.3450-09.2009
1:
2560:10.1016/S0896-6273(00)81072-7
1338:Annual Review of Neuroscience
1076:Behavioral and Brain Sciences
1036:10.1016/S0896-6273(00)80773-4
539:Place cells were reported in
4635:10.1371/journal.pbio.3000546
4579:10.1016/j.neulet.2019.02.009
4528:10.1016/0304-3940(91)90683-K
3758:10.1007/978-3-7091-1292-2_16
3540:10.1016/j.neuron.2018.07.047
2832:Jeffery, Kathryn J. (2003).
2780:Reviews in the Neurosciences
1952:10.1016/0301-0082(79)90005-4
1575:10.1016/j.neuron.2018.10.002
980:10.1016/0014-4886(76)90055-8
883:10.1016/0006-8993(71)90358-1
383:Morris water navigation task
4950:Nature Reviews Neuroscience
4143:Nature Reviews Neuroscience
3631:Nature Reviews Neuroscience
3405:Nature Reviews Neuroscience
3189:Nature Reviews Neuroscience
2838:. Oxford University Press.
2109:The Journal of Neuroscience
1991:Experimental Brain Research
1889:Nature Reviews Neuroscience
711:The Journal of Neuroscience
448:Dentate gyrus § Memory
401:, a process which sums the
5122:
3305:10.1016/j.conb.2005.10.002
2934:10.1038/s41467-018-03262-4
2385:10.1016/j.conb.2011.07.002
2062:10.1016/j.tins.2008.06.008
1688:10.1038/s41467-019-13760-8
1623:10.1016/j.tins.2013.12.003
467:
445:
259:
180:Relationship to grid cells
114:chronic electrode implants
3417:10.1038/s41583-018-0077-1
3360:10.1016/j.cub.2017.10.073
3237:Rolls, Edmund T. (2013).
1088:10.1017/s0140525x00063949
5025:10.3389/fnagi.2010.00026
3930:10.3389/fncel.2018.00332
3256:10.3389/fnsys.2013.00074
3033:10.3389/fnint.2014.00038
2171:10.3389/fnbeh.2017.00253
1940:Progress in Neurobiology
290:successor representation
243:two types of remapping:
4796:10.1073/pnas.0802908105
4409:10.1126/science.aao3474
4294:10.1126/science.1235338
4111:10.1126/science.aao3898
4033:Journal of Neuroscience
3871:10.1126/science.8351520
2433:Journal of Neuroscience
2224:Journal of Neuroscience
2049:Trends in Neurosciences
1611:Trends in Neurosciences
1158:Journal of Neuroscience
582:
2335:10.1002/hipo.450030307
1745:10.1098/rstb.1998.0287
1284:10.1002/hipo.450010207
1119:Psychological Bulletin
968:Experimental Neurology
847:. Karolinska Institute
680:O'Keefe, John (1978).
508:
406:
322:
234:
200:
176:
137:
42:
2914:Nature Communications
2877:10.1093/cercor/bht239
1803:10.1073/pnas.94.1.343
1668:Nature Communications
506:
396:
311:hippocampal formation
308:
232:
198:
171:
134:
99:for the discovery of
35:
5082:at Wikimedia Commons
4567:Neuroscience Letters
4516:Neuroscience Letters
657:Head direction cells
481:memory consolidation
458:competitive learning
153:of the environment.
5096:Hippocampus (brain)
4787:2008PNAS..105.7863C
4400:2018Sci...359..218O
4333:Nature Neuroscience
4286:2013Sci...340..367Y
4252:Scientific American
4194:Nature Neuroscience
4155:10.1038/nrn.2018.12
4102:2018Sci...359..213D
4039:(46): 14521–14533.
3976:Nature Neuroscience
3863:1993Sci...261.1055W
3857:(5124): 1055–1058.
3812:10.1038/nature01964
3794:2003Natur.425..184E
3589:10.1155/2011/203462
3533:(6): 1329–1341.e6.
3482:10.1038/nature09633
3474:2011Natur.469..397D
2926:2018NatCo...9..839R
2692:10.7554/eLife.44487
2490:Nature Neuroscience
1794:1997PNAS...94..343B
1680:2019NatCo..10.5685M
1507:Nature Neuroscience
1456:10.1038/nature21692
1448:2017Natur.543..719A
930:2014Natur.514..153A
684:. Clarendon Press.
626:glutamate receptors
593:Alzheimer's disease
583:Alzheimer's disease
541:Egyptian fruit bats
338:Visuospatial inputs
270:, a process termed
4909:10.1002/hipo.22283
4854:10.1002/hipo.22697
3698:10.1002/hipo.20108
3153:10.1002/hipo.20208
2982:10.1002/hipo.20588
2643:10.1002/hipo.20322
2294:10.1007/BF03337772
2003:10.1007/BF00237147
1233:10.1002/hipo.10173
779:10.1002/hipo.20322
646:Spatial view cells
574:Effects of alcohol
562:spatial view cells
509:
470:Hippocampal replay
442:Pattern separation
433:Pattern completion
407:
323:
235:
201:
177:
138:
43:
5106:Spatial cognition
5078:Media related to
4781:(22): 7863–7868.
4734:(10): 1986–1997.
4394:(6372): 218–224.
4280:(6130): 367–372.
4254:. Nature Magazine
4096:(6372): 213–218.
3982:(11): 1433–1440.
3788:(6954): 184–188.
3767:978-3-7091-1292-2
3576:Neural Plasticity
3468:(7330): 397–401.
3081:(11): 2206–2219.
2845:978-0-19-851524-1
2496:(11): 1433–1440.
2439:(12): 7235–7251.
2230:(26): 8827–8835.
1739:(1373): 1333–40.
1513:(11): 1643–1653.
1442:(7647): 719–722.
1164:(14): 6254–6264.
717:(11): 4016–4025.
371:vestibular system
369:Stimuli from the
365:Vestibular inputs
328:entorhinal cortex
315:entorhinal cortex
132:
16:(Redirected from
5113:
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4672:
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4637:
4628:(12): e3000546.
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3333:
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3278:
3268:
3258:
3234:
3221:
3220:
3184:
3173:
3172:
3146:
3126:
3115:
3114:
3070:
3064:
3063:
3053:
3035:
3011:
3002:
3001:
2965:
2956:
2955:
2945:
2905:
2899:
2898:
2888:
2856:
2850:
2849:
2829:
2820:
2819:
2775:
2769:
2768:
2732:
2723:
2722:
2712:
2694:
2669:
2663:
2662:
2626:
2620:
2619:
2594:(9): 1696–1705.
2579:
2573:
2572:
2562:
2538:
2532:
2531:
2521:
2481:
2475:
2474:
2464:
2424:
2415:
2414:
2404:
2364:
2355:
2354:
2318:
2307:
2306:
2296:
2272:
2266:
2265:
2255:
2215:
2202:
2201:
2191:
2173:
2149:
2143:
2142:
2132:
2100:
2091:
2090:
2064:
2040:
2031:
2030:
1986:
1980:
1979:
1935:
1929:
1928:
1884:
1878:
1877:
1841:
1826:
1825:
1815:
1805:
1773:
1767:
1766:
1756:
1724:
1718:
1717:
1707:
1659:
1653:
1652:
1642:
1602:
1596:
1595:
1577:
1553:
1547:
1546:
1504:
1495:
1486:
1485:
1475:
1427:
1418:
1417:
1381:
1370:
1369:
1333:
1312:
1311:
1267:
1261:
1260:
1226:
1206:
1200:
1199:
1189:
1149:
1143:
1142:
1131:10.1037/a0022315
1114:
1108:
1107:
1071:
1065:
1064:
1038:
1014:
1008:
1007:
963:
952:
951:
941:
909:
903:
902:
866:
857:
856:
854:
852:
846:
837:
831:
830:
828:
827:
813:
807:
806:
762:
745:
744:
734:
702:
696:
695:
677:
620:that blocks the
554:Japanese macaque
477:memory retrieval
411:path integration
399:path integration
356:Olfactory inputs
313:, including the
272:phase precession
262:Phase precession
256:Phase precession
215:receptive fields
190:Hebbian learning
133:
51:pyramidal neuron
21:
5121:
5120:
5116:
5115:
5114:
5112:
5111:
5110:
5086:
5085:
5070:
5065:
5048:
5005:
5004:
4993:
4962:10.1038/nrn1809
4947:
4946:
4942:
4890:
4889:
4885:
4838:
4837:
4830:
4768:
4767:
4763:
4725:
4724:
4720:
4674:
4673:
4669:
4615:
4614:
4610:
4564:
4563:
4559:
4513:
4512:
4508:
4462:
4461:
4457:
4448:
4446:
4438:
4437:
4433:
4381:
4380:
4376:
4345:10.1038/nn.4310
4330:
4329:
4325:
4271:
4270:
4266:
4257:
4255:
4245:
4244:
4237:
4191:
4190:
4186:
4140:
4139:
4135:
4083:
4082:
4078:
4026:
4025:
4021:
3988:10.1038/nn.2648
3969:
3968:
3964:
3910:
3909:
3902:
3848:
3847:
3843:
3803:10.1.1.408.4443
3779:
3778:
3774:
3768:
3747:
3746:
3729:
3682:
3681:
3674:
3643:10.1038/nrn3888
3628:
3627:
3623:
3569:
3568:
3564:
3520:
3519:
3515:
3455:
3454:
3450:
3411:(12): 744–757.
3398:
3397:
3393:
3348:Current Biology
3341:
3340:
3336:
3290:
3289:
3282:
3236:
3235:
3224:
3201:10.1038/nrn1385
3186:
3185:
3176:
3144:10.1.1.141.1450
3128:
3127:
3118:
3072:
3071:
3067:
3013:
3012:
3005:
2967:
2966:
2959:
2907:
2906:
2902:
2865:Cerebral Cortex
2858:
2857:
2853:
2846:
2831:
2830:
2823:
2786:(2–3): 95–112.
2777:
2776:
2772:
2734:
2733:
2726:
2671:
2670:
2666:
2628:
2627:
2623:
2581:
2580:
2576:
2540:
2539:
2535:
2502:10.1038/nn.2648
2483:
2482:
2478:
2426:
2425:
2418:
2366:
2365:
2358:
2320:
2319:
2310:
2274:
2273:
2269:
2217:
2216:
2205:
2151:
2150:
2146:
2102:
2101:
2094:
2042:
2041:
2034:
1988:
1987:
1983:
1937:
1936:
1932:
1901:10.1038/nrn3888
1886:
1885:
1881:
1843:
1842:
1829:
1775:
1774:
1770:
1726:
1725:
1721:
1661:
1660:
1656:
1604:
1603:
1599:
1555:
1554:
1550:
1519:10.1038/nn.4650
1502:
1497:
1496:
1489:
1429:
1428:
1421:
1383:
1382:
1373:
1335:
1334:
1315:
1269:
1268:
1264:
1224:10.1.1.463.1315
1208:
1207:
1203:
1151:
1150:
1146:
1116:
1115:
1111:
1073:
1072:
1068:
1016:
1015:
1011:
965:
964:
955:
939:10.1038/514153a
911:
910:
906:
868:
867:
860:
850:
848:
844:
839:
838:
834:
825:
823:
815:
814:
810:
764:
763:
748:
704:
703:
699:
692:
679:
678:
674:
670:
642:
601:
585:
576:
571:
558:common marmoset
550:
537:
514:
497:
472:
466:
450:
444:
435:
427:episodic memory
423:
421:Episodic memory
391:
389:Movement inputs
379:radial arm maze
367:
358:
340:
309:Anatomy of the
299:
285:radial arm maze
280:
264:
258:
240:
211:
206:
182:
124:
118:extracellularly
109:
97:May-Britt Moser
87:was awarded to
74:episodic memory
28:
23:
22:
15:
12:
11:
5:
5119:
5117:
5109:
5108:
5103:
5098:
5088:
5087:
5084:
5083:
5069:
5068:External links
5066:
5064:
5063:
4991:
4940:
4903:(8): 963–978.
4883:
4848:(4): 378–392.
4828:
4761:
4718:
4667:
4608:
4557:
4522:(1): 194–198.
4506:
4471:(4): 467–480.
4455:
4431:
4374:
4339:(7): 952–958.
4323:
4264:
4235:
4206:10.1038/nn1829
4200:(2): 224–233.
4184:
4133:
4076:
4019:
3962:
3900:
3841:
3772:
3766:
3727:
3692:(8): 991–996.
3672:
3621:
3562:
3513:
3448:
3391:
3354:(1): R37–R50.
3334:
3299:(6): 738–746.
3280:
3222:
3195:(5): 368–369.
3174:
3137:(9): 716–729.
3116:
3065:
3003:
2957:
2900:
2871:(2): 423–432.
2851:
2844:
2821:
2770:
2724:
2664:
2637:(9): 775–785.
2621:
2574:
2553:(3): 707–715.
2533:
2476:
2416:
2379:(5): 734–744.
2356:
2308:
2287:(3): 221–227.
2267:
2203:
2144:
2115:(7): 1951–68.
2092:
2055:(9): 469–477.
2032:
1981:
1946:(4): 419–439.
1930:
1879:
1852:(2): 201–218.
1827:
1788:(1): 343–350.
1768:
1719:
1654:
1617:(3): 136–145.
1597:
1568:(2): 490–509.
1548:
1487:
1419:
1392:(4): 352–364.
1371:
1313:
1278:(2): 193–205.
1262:
1217:(2): 180–192.
1201:
1144:
1125:(3): 484–507.
1109:
1082:(4): 487–533.
1066:
1029:(2): 209–226.
1009:
953:
904:
877:(1): 171–175.
871:Brain Research
858:
832:
821:Nobelprize.org
808:
773:(9): 775–785.
746:
697:
691:978-0198572060
690:
671:
669:
666:
665:
664:
659:
654:
649:
641:
638:
622:NMDA receptors
600:
597:
589:spatial memory
587:Problems with
584:
581:
575:
572:
570:
567:
549:
546:
536:
533:
513:
510:
496:
493:
468:Main article:
465:
462:
443:
440:
434:
431:
422:
419:
390:
387:
366:
363:
357:
354:
339:
336:
298:
295:
279:
278:Directionality
276:
260:Main article:
257:
254:
247:remapping and
239:
236:
210:
207:
205:
202:
181:
178:
147:misplace units
108:
105:
26:
24:
14:
13:
10:
9:
6:
4:
3:
2:
5118:
5107:
5104:
5102:
5099:
5097:
5094:
5093:
5091:
5081:
5076:
5072:
5071:
5067:
5059:
5053:
5045:
5041:
5036:
5031:
5026:
5021:
5017:
5013:
5009:
5002:
5000:
4998:
4996:
4992:
4987:
4983:
4979:
4975:
4971:
4967:
4963:
4959:
4955:
4951:
4944:
4941:
4936:
4932:
4927:
4922:
4918:
4914:
4910:
4906:
4902:
4898:
4894:
4887:
4884:
4879:
4875:
4871:
4867:
4863:
4859:
4855:
4851:
4847:
4843:
4835:
4833:
4829:
4824:
4820:
4815:
4810:
4806:
4802:
4797:
4792:
4788:
4784:
4780:
4776:
4772:
4765:
4762:
4757:
4753:
4749:
4745:
4741:
4737:
4733:
4729:
4722:
4719:
4714:
4710:
4706:
4702:
4698:
4694:
4690:
4686:
4682:
4678:
4671:
4668:
4663:
4659:
4654:
4649:
4645:
4641:
4636:
4631:
4627:
4623:
4619:
4612:
4609:
4604:
4600:
4596:
4592:
4588:
4584:
4580:
4576:
4572:
4568:
4561:
4558:
4553:
4549:
4545:
4541:
4537:
4533:
4529:
4525:
4521:
4517:
4510:
4507:
4502:
4498:
4494:
4490:
4486:
4482:
4478:
4474:
4470:
4466:
4459:
4456:
4445:
4441:
4435:
4432:
4427:
4423:
4419:
4415:
4410:
4405:
4401:
4397:
4393:
4389:
4385:
4378:
4375:
4370:
4366:
4362:
4358:
4354:
4350:
4346:
4342:
4338:
4334:
4327:
4324:
4319:
4315:
4311:
4307:
4303:
4299:
4295:
4291:
4287:
4283:
4279:
4275:
4268:
4265:
4253:
4249:
4242:
4240:
4236:
4231:
4227:
4223:
4219:
4215:
4211:
4207:
4203:
4199:
4195:
4188:
4185:
4180:
4176:
4172:
4168:
4164:
4160:
4156:
4152:
4148:
4144:
4137:
4134:
4129:
4125:
4121:
4117:
4112:
4107:
4103:
4099:
4095:
4091:
4087:
4080:
4077:
4072:
4068:
4063:
4058:
4054:
4050:
4046:
4042:
4038:
4034:
4030:
4023:
4020:
4015:
4011:
4006:
4001:
3997:
3993:
3989:
3985:
3981:
3977:
3973:
3966:
3963:
3958:
3954:
3949:
3944:
3940:
3936:
3931:
3926:
3922:
3918:
3914:
3907:
3905:
3901:
3896:
3892:
3888:
3884:
3880:
3876:
3872:
3868:
3864:
3860:
3856:
3852:
3845:
3842:
3837:
3833:
3829:
3825:
3821:
3817:
3813:
3809:
3804:
3799:
3795:
3791:
3787:
3783:
3776:
3773:
3769:
3763:
3759:
3755:
3751:
3744:
3742:
3740:
3738:
3736:
3734:
3732:
3728:
3723:
3719:
3715:
3711:
3707:
3703:
3699:
3695:
3691:
3687:
3679:
3677:
3673:
3668:
3664:
3660:
3656:
3652:
3648:
3644:
3640:
3637:(2): 94–108.
3636:
3632:
3625:
3622:
3617:
3613:
3608:
3603:
3599:
3595:
3590:
3585:
3581:
3577:
3573:
3566:
3563:
3558:
3554:
3550:
3546:
3541:
3536:
3532:
3528:
3524:
3517:
3514:
3509:
3505:
3500:
3495:
3491:
3487:
3483:
3479:
3475:
3471:
3467:
3463:
3459:
3452:
3449:
3444:
3440:
3435:
3430:
3426:
3422:
3418:
3414:
3410:
3406:
3402:
3395:
3392:
3387:
3383:
3378:
3373:
3369:
3365:
3361:
3357:
3353:
3349:
3345:
3338:
3335:
3330:
3326:
3322:
3318:
3314:
3310:
3306:
3302:
3298:
3294:
3287:
3285:
3281:
3276:
3272:
3267:
3262:
3257:
3252:
3248:
3244:
3240:
3233:
3231:
3229:
3227:
3223:
3218:
3214:
3210:
3206:
3202:
3198:
3194:
3190:
3183:
3181:
3179:
3175:
3170:
3166:
3162:
3158:
3154:
3150:
3145:
3140:
3136:
3132:
3125:
3123:
3121:
3117:
3112:
3108:
3104:
3100:
3096:
3092:
3088:
3084:
3080:
3076:
3069:
3066:
3061:
3057:
3052:
3047:
3043:
3039:
3034:
3029:
3025:
3021:
3017:
3010:
3008:
3004:
2999:
2995:
2991:
2987:
2983:
2979:
2975:
2971:
2964:
2962:
2958:
2953:
2949:
2944:
2939:
2935:
2931:
2927:
2923:
2919:
2915:
2911:
2904:
2901:
2896:
2892:
2887:
2882:
2878:
2874:
2870:
2866:
2862:
2855:
2852:
2847:
2841:
2837:
2836:
2828:
2826:
2822:
2817:
2813:
2809:
2805:
2801:
2797:
2793:
2789:
2785:
2781:
2774:
2771:
2766:
2762:
2758:
2754:
2750:
2746:
2742:
2738:
2731:
2729:
2725:
2720:
2716:
2711:
2706:
2702:
2698:
2693:
2688:
2684:
2680:
2676:
2668:
2665:
2660:
2656:
2652:
2648:
2644:
2640:
2636:
2632:
2625:
2622:
2617:
2613:
2609:
2605:
2601:
2597:
2593:
2589:
2585:
2578:
2575:
2570:
2566:
2561:
2556:
2552:
2548:
2544:
2537:
2534:
2529:
2525:
2520:
2515:
2511:
2507:
2503:
2499:
2495:
2491:
2487:
2480:
2477:
2472:
2468:
2463:
2458:
2454:
2450:
2446:
2442:
2438:
2434:
2430:
2423:
2421:
2417:
2412:
2408:
2403:
2398:
2394:
2390:
2386:
2382:
2378:
2374:
2370:
2363:
2361:
2357:
2352:
2348:
2344:
2340:
2336:
2332:
2329:(3): 317–30.
2328:
2324:
2317:
2315:
2313:
2309:
2304:
2300:
2295:
2290:
2286:
2282:
2281:Psychobiology
2278:
2271:
2268:
2263:
2259:
2254:
2249:
2245:
2241:
2237:
2233:
2229:
2225:
2221:
2214:
2212:
2210:
2208:
2204:
2199:
2195:
2190:
2185:
2181:
2177:
2172:
2167:
2163:
2159:
2155:
2148:
2145:
2140:
2136:
2131:
2126:
2122:
2118:
2114:
2110:
2106:
2099:
2097:
2093:
2088:
2084:
2080:
2076:
2072:
2068:
2063:
2058:
2054:
2050:
2046:
2039:
2037:
2033:
2028:
2024:
2020:
2016:
2012:
2008:
2004:
2000:
1996:
1992:
1985:
1982:
1977:
1973:
1969:
1965:
1961:
1957:
1953:
1949:
1945:
1941:
1934:
1931:
1926:
1922:
1918:
1914:
1910:
1906:
1902:
1898:
1895:(2): 94–108.
1894:
1890:
1883:
1880:
1875:
1871:
1867:
1863:
1859:
1855:
1851:
1847:
1840:
1838:
1836:
1834:
1832:
1828:
1823:
1819:
1814:
1809:
1804:
1799:
1795:
1791:
1787:
1783:
1779:
1772:
1769:
1764:
1760:
1755:
1750:
1746:
1742:
1738:
1734:
1730:
1723:
1720:
1715:
1711:
1706:
1701:
1697:
1693:
1689:
1685:
1681:
1677:
1673:
1669:
1665:
1658:
1655:
1650:
1646:
1641:
1636:
1632:
1628:
1624:
1620:
1616:
1612:
1608:
1601:
1598:
1593:
1589:
1585:
1581:
1576:
1571:
1567:
1563:
1559:
1552:
1549:
1544:
1540:
1536:
1532:
1528:
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1520:
1516:
1512:
1508:
1501:
1494:
1492:
1488:
1483:
1479:
1474:
1469:
1465:
1461:
1457:
1453:
1449:
1445:
1441:
1437:
1433:
1426:
1424:
1420:
1415:
1411:
1407:
1403:
1399:
1395:
1391:
1387:
1380:
1378:
1376:
1372:
1367:
1363:
1359:
1355:
1351:
1347:
1343:
1339:
1332:
1330:
1328:
1326:
1324:
1322:
1320:
1318:
1314:
1309:
1305:
1301:
1297:
1293:
1289:
1285:
1281:
1277:
1273:
1266:
1263:
1258:
1254:
1250:
1246:
1242:
1238:
1234:
1230:
1225:
1220:
1216:
1212:
1205:
1202:
1197:
1193:
1188:
1183:
1179:
1175:
1171:
1167:
1163:
1159:
1155:
1148:
1145:
1140:
1136:
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1128:
1124:
1120:
1113:
1110:
1105:
1101:
1097:
1093:
1089:
1085:
1081:
1077:
1070:
1067:
1062:
1058:
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1028:
1024:
1020:
1013:
1010:
1005:
1001:
997:
993:
989:
985:
981:
977:
974:(1): 78–109.
973:
969:
962:
960:
958:
954:
949:
945:
940:
935:
931:
927:
924:(7521): 153.
923:
919:
915:
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884:
880:
876:
872:
865:
863:
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623:
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563:
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555:
547:
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532:
530:
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505:
501:
495:Model animals
494:
492:
490:
486:
482:
478:
471:
463:
461:
459:
455:
454:dentate gyrus
449:
441:
439:
432:
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416:
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372:
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355:
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350:
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333:
329:
320:
319:dentate gyrus
316:
312:
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297:Sensory input
296:
294:
291:
286:
277:
275:
273:
269:
263:
255:
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237:
231:
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216:
208:
203:
197:
193:
191:
187:
179:
174:
170:
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151:cognitive map
148:
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79:
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63:cognitive map
60:
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52:
49:is a kind of
48:
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5052:cite journal
5015:
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4956:(1): 30–40.
4953:
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4764:
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4683:(1): 88–93.
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4625:
4622:PLOS Biology
4621:
4611:
4570:
4566:
4560:
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4443:
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4251:
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3188:
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3023:
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2976:(1): 36–43.
2973:
2969:
2917:
2913:
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2864:
2854:
2834:
2783:
2779:
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2630:
2624:
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1997:(1): 41–49.
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1933:
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1600:
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851:September 7,
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209:Place fields
183:
163:
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142:place units.
141:
139:
110:
89:John O'Keefe
82:
71:
67:
46:
44:
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5080:Place cells
4897:Hippocampus
4842:Hippocampus
4677:Hippocampus
4465:Hippocampus
3686:Hippocampus
3131:Hippocampus
2970:Hippocampus
2737:Hippocampus
2631:Hippocampus
2323:Hippocampus
1674:(1): 5685.
1386:Hippocampus
1272:Hippocampus
1211:Hippocampus
918:Nature News
767:Hippocampus
522:chinchillas
268:theta waves
224:allocentric
59:place field
55:hippocampus
18:Place cells
5090:Categories
4449:2020-01-03
4258:2020-01-03
4149:(3): 122.
3582:: 203462.
2920:(1): 839.
2685:: e44487.
826:2014-10-06
668:References
652:Grid cells
618:antagonist
485:prediction
446:See also:
415:grid cells
349:contextual
317:(EC), the
204:Properties
186:grid cells
173:Grid cells
107:Background
101:grid cells
47:place cell
41:potential.
4970:1471-0048
4917:1098-1063
4862:1098-1063
4805:0027-8424
4728:Neurology
4697:1098-1063
4644:1545-7885
4587:0304-3940
4573:: 32–37.
4536:0304-3940
4485:1098-1063
4418:0036-8075
4353:1546-1726
4302:0036-8075
4214:1546-1726
4163:1471-0048
4120:0036-8075
4053:0270-6474
3996:1546-1726
3939:1662-5102
3879:0036-8075
3820:1476-4687
3798:CiteSeerX
3706:1098-1063
3651:1471-0048
3598:2090-5904
3490:0028-0836
3425:1471-0048
3368:0960-9822
3313:0959-4388
3139:CiteSeerX
3095:0953-816X
3042:1662-5145
2800:2191-0200
2701:2050-084X
2510:1546-1726
2453:0270-6474
2393:0959-4388
2303:0889-6313
2244:0270-6474
2180:1662-5153
2071:0166-2236
2011:1432-1106
1960:0301-0082
1909:1471-0048
1696:2041-1723
1631:0166-2236
1584:0896-6273
1543:205441266
1527:1546-1726
1464:0028-0836
1292:1098-1063
1241:1098-1063
1219:CiteSeerX
1178:0270-6474
1104:616519952
1096:144038992
1045:0896-6273
988:0014-4886
891:0006-8993
803:621877128
614:memantine
375:Bilateral
332:olfactory
238:Remapping
158:landmarks
83:The 2014
5044:20802800
4978:16371948
4935:24752989
4870:28032686
4823:18505838
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4595:30738872
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4493:10495028
4444:phys.org
4426:29326274
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1406:10495018
1366:16036900
1358:18284371
1308:31246290
1249:15098724
1196:12122084
1139:21299273
1100:ProQuest
1053:10399928
948:25297415
799:ProQuest
787:17615579
741:11356888
640:See also
630:encoding
548:Primates
489:learning
381:and the
5101:Neurons
5035:2928699
4986:1784238
4926:4456091
4878:2904174
4814:2396558
4783:Bibcode
4653:6922474
4544:2020375
4501:7685147
4396:Bibcode
4388:Science
4282:Bibcode
4274:Science
4230:9181649
4179:3267792
4098:Bibcode
4090:Science
4062:2821030
4005:2967725
3948:6160568
3923:: 332.
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3859:Bibcode
3851:Science
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3377:5847173
3329:9770011
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3217:7728258
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2922:Bibcode
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2253:6740394
2189:5758554
2164:: 253.
2139:3612226
2130:6568940
2027:6193356
2019:6628596
1976:8022838
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1790:Bibcode
1763:9770226
1754:1692339
1705:6908717
1676:Bibcode
1640:3945817
1473:5492514
1444:Bibcode
1414:1961703
1300:1669293
1257:1646974
1187:6757929
1061:8518920
1004:1113367
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926:Bibcode
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795:3141473
732:6762702
529:Science
512:Rodents
403:vectors
249:partial
53:in the
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245:global
220:bursts
93:Edvard
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4752:S2CID
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4365:S2CID
4314:S2CID
4226:S2CID
4175:S2CID
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3832:S2CID
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3165:S2CID
3107:S2CID
2994:S2CID
2812:S2CID
2761:S2CID
2679:eLife
2655:S2CID
2612:S2CID
2347:S2CID
2083:S2CID
2023:S2CID
1972:S2CID
1921:S2CID
1870:S2CID
1813:19339
1539:S2CID
1503:(PDF)
1410:S2CID
1362:S2CID
1304:S2CID
1253:S2CID
1092:S2CID
1057:S2CID
1000:S2CID
845:(PDF)
791:S2CID
616:, an
599:Aging
136:cell.
5058:link
5040:PMID
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853:2018
783:PMID
737:PMID
686:ISBN
556:and
535:Bats
487:and
479:and
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4648:PMC
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