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Jeffrey S. Taube - One of the best experts on this subject based on the ideXlab platform.
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Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016Co-Authors: Stephane Valerio, Jeffrey S. TaubeAbstract:Head Direction (HD) Cells fire when an animal faces a particular Direction in its environment, and they are thought to represent the neural correlate of the animal's perceived spatial orientation. Previous studies have shown that vestibular information is critical for generating the HD signal but have not delineated whether information from all three semicircular canals or just the horizontal canals, which are primarily sensitive to angular Head rotation in the horizontal (yaw) plane, are critical for the signal. Here, we monitored cell activity in the anterodorsal thalamus (ADN), an area known to contain HD Cells, in epstatic circler (Ecl) mice, which have a bilateral malformation of the horizontal (lateral) semicircular canals. Ecl mice and their littermates that did not express the mutation (controls) were implanted with recording electrodes in the ADN. Results confirm the important role the horizontal canals play in forming the HD signal. Although normal HD cell activity (Raleigh's r > 0.4) was recorded in control mice, no such activity was found in Ecl mice, although some Cells had activity that was mildly modulated by HD (0.4 > r > 0.2). Importantly, we also observed activity in Ecl mice that was best characterized as bursty--a pattern of activity similar to an HD signal but without any preferred firing Direction. These results suggest that the neural structure for the HD network remains intact in Ecl mice, but the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable HD signal. Significance statement: Cells in the anterior dorsal thalamic nucleus normally fire in relation to the animal's Directional Heading with respect to the environment--so-called Head Direction Cells. To understand how these Head Direction Cells generate their activity, we recorded single-unit activity from the anterior dorsal thalamus in transgenic mice that lack functional horizontal semicircular canals. We show that the neural network for the Head Direction signal remains intact in these mice, but that the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable Head Direction signal.
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the vestibular contribution to the Head Direction signal and navigation
Frontiers in Integrative Neuroscience, 2014Co-Authors: Ryan M Yoder, Jeffrey S. TaubeAbstract:Spatial learning and navigation depend on neural representations of location and Direction within the environment. These representations, encoded by place Cells and Head Direction Cells, respectively, are dominantly controlled by visual cues, but require input from the vestibular system. Vestibular signals play an important role in forming spatial representations in both visual and non-visual environments, but the details of this vestibular contribution are not fully understood. Here, we review the role of the vestibular system in generating various spatial signals in rodents, focusing primarily on Head Direction Cells. We also examine the vestibular system’s role in navigation and the possible pathways by which vestibular information is conveyed to higher navigation centers.
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updating of the spatial reference frame of Head Direction Cells in response to locomotion in the vertical plane
Journal of Neurophysiology, 2013Co-Authors: Jeffrey S. Taube, Sarah S Wang, Stanley Y Kim, Russell J FrohardtAbstract:Many species navigate in three dimensions and are required to maintain accurate orientation while moving in an Earth vertical plane. Here we explored how Head Direction (HD) Cells in the rat antero...
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path integration how the Head Direction signal maintains and corrects spatial orientation
Nature Neuroscience, 2012Co-Authors: Stephane Valerio, Jeffrey S. TaubeAbstract:Path integration allows animals to track their body position in planar space by relying on both external cues and internal cues. For monitoring internal cues, Head Direction Cells in the anterodorsal thalamic nucleus are one of the best candidates for the neural mechanism underlying path integration. This study shows that Head-Direction Cells in rats act as a mediator of path integration such that their firing matches the level of movement trajectory Heading errors in a cumulative manner, and that Head-Direction Cells correct their firing when internal error is corrected by external cues.
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projections to the anterodorsal thalamus and lateral mammillary nuclei arise from different cell populations within the postsubiculum implications for the control of Head Direction Cells
Hippocampus, 2011Co-Authors: Ryan M Yoder, Jeffrey S. TaubeAbstract:The neural representation of Directional Heading is encoded by a population of Cells located in a circuit that includes the postsubiculum (PoS), anterodorsal thalamus (ADN), and lateral mammillary nuclei (LMN). Throughout this circuit, many Cells rely on both movement- and landmark-related information to discharge as a function of the animal's Directional Heading. The PoS projects to both the ADN and LMN, and these connections may convey critical spatial information about landmarks, because lesions of the PoS disrupt landmark control in Head Direction (HD) Cells and hippocampal place Cells [Goodridge and Taube (1997) J Neurosci 17:9315-9330; Calton et al. (2003) J Neurosci 23:9719-9731]. The PoS → ADN projection originates in the deep layers of PoS, but no studies have determined whether the PoS → LMN projection originates from the same Cells that project to ADN. To address this issue, two distinct cholera toxin-subunit B (CTB) fluorophore conjugates (Alexa Fluor 488 and Alexa Fluor 594) were injected into the LMN and ADN of the same rats, and PoS sections were examined for cell bodies containing either or both CTB conjugates. Results indicated that the PoS → LMN projection originates exclusively from a thin layer of Cells located superficial to the layer(s) of PoS → ADN projection Cells, with no overlap. To verify the laminar distribution and morphological characteristics of PoS → LMN and PoS → ADN Cells, biotinylated dextran amine was injected into LMN or ADN of different rats, and tissue sections were counterstained with thionin. Results indicated that the PoS → LMN projection arises from large pyramidal Cells in layer IV, whereas the PoS → ADN projection arises from a heterogeneous cell population in layers V/VI. This study provides the first evidence that the PoS → ADN and PoS → LMN projections arise from distinct, nonoverlapping cell layers in PoS. Functionally, the PoS may provide landmark information to HD Cells in LMN.
Edvard I. Moser - One of the best experts on this subject based on the ideXlab platform.
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spatial representation in the hippocampal formation a history
Nature Neuroscience, 2017Co-Authors: Edvard I. Moser, Bruce L McnaughtonAbstract:Since the first place cell was recorded and the cognitive-map theory was subsequently formulated, investigation of spatial representation in the hippocampal formation has evolved in stages. Early studies sought to verify the spatial nature of place cell activity and determine its sensory origin. A new epoch started with the discovery of Head Direction Cells and the realization of the importance of angular and linear movement-integration in generating spatial maps. A third epoch began when investigators turned their attention to the entorhinal cortex, which led to the discovery of grid Cells and border Cells. This review will show how ideas about integration of self-motion cues have shaped our understanding of spatial representation in hippocampal-entorhinal systems from the 1970s until today. It is now possible to investigate how specialized cell types of these systems work together, and spatial mapping may become one of the first cognitive functions to be understood in mechanistic detail.
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Parvalbumin and Somatostatin Interneurons Control Different Space-Coding Networks in the Medial Entorhinal Cortex
Cell, 2017Co-Authors: Chenglin Miao, Maybritt Moser, Qichen Cao, Edvard I. MoserAbstract:Summary The medial entorhinal cortex (MEC) contains several discrete classes of GABAergic interneurons, but their specific contributions to spatial pattern formation in this area remain elusive. We employed a pharmacogenetic approach to silence either parvalbumin (PV)- or somatostatin (SOM)-expressing interneurons while MEC Cells were recorded in freely moving mice. PV-cell silencing antagonized the hexagonally patterned spatial selectivity of grid Cells, especially in layer II of MEC. The impairment was accompanied by reduced speed modulation in colocalized speed Cells. Silencing SOM Cells, in contrast, had no impact on grid Cells or speed Cells but instead decreased the spatial selectivity of Cells with discrete aperiodic firing fields. Border Cells and Head Direction Cells were not affected by either intervention. The findings point to distinct roles for PV and SOM interneurons in the local dynamics underlying periodic and aperiodic firing in spatially modulated Cells of the MEC. Video Abstract
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grid Cells and spatial maps in entorhinal cortex and hippocampus
2016Co-Authors: Tor Stensola, Edvard I. MoserAbstract:The cortical circuit for spatial representation has multiple functionally distinct components, each dedicated to a highly specific aspect of spatial processing. The circuit includes place Cells in the hippocampus as well as grid Cells, Head Direction Cells and border Cells in the medial entorhinal cortex. In this review we discuss the functional organization of the hippocampal-entorhinal space circuit. We shall review data suggesting that the circuit of grid Cells has a modular organization and we will discuss principles by which individual modules of grid Cells interact with geometric features of the external environment. We shall argue that the modular organization of the grid-cell system may be instrumental in memory orthogonalization in place Cells in the hippocampus. Taken together, these examples illustrate a brain system that performs computations at the highest level, yet remains one of the cortical circuits with the best readout for experimental analysis and intervention.
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representation of geometric borders in the developing rat
Neuron, 2014Co-Authors: Tale Litlere Bjerknes, Edvard I. Moser, Maybritt MoserAbstract:Summary Local space is represented by a number of functionally specific cell types, including place Cells in the hippocampus and grid Cells, Head Direction Cells, and border Cells in the medial entorhinal cortex (MEC). These Cells form a functional map of external space already at the time when rat pups leave the nest for the first time in their life, at the age of 2.5 weeks. However, while place Cells have adult-like firing fields from the outset, grid Cells have irregular and variable fields until the fourth week, raising doubts about their contribution to place cell firing at young age. Recording in MEC of juvenile rats, we show that, unlike grid Cells, border Cells express adult-like firing fields from the first days of exposure to an open environment, at postnatal days 16–18. Thus, spatial signals from border Cells may be sufficient to maintain spatially localized firing in juvenile hippocampal place Cells.
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Topography of Head Direction Cells in Medial Entorhinal Cortex
Current Biology, 2014Co-Authors: Lisa M. Giocomo, Maybritt Moser, Tiffany Van Cauter, Tor Stensola, Tora Bonnevie, Edvard I. MoserAbstract:Summary Background Neural circuits in the medial entorhinal cortex (MEC) support translation of the external environment to an internal map of space, with grid and Head Direction neurons providing metrics for distance and orientation. Results We show here that Head Direction Cells in MEC are organized topographically. Head Direction tuning varies widely across the entire dorsoventral MEC axis, but in layer III there is a gradual dorsal-to-ventral increase in the average width of the Directional firing field. Sharply tuned Cells were encountered only at the dorsal end of MEC. Similar topography was not observed among Head Direction Cells in layers V–VI. At all MEC locations, in all layers, the preferred firing Direction (Directional phase) showed a uniform distribution. The continuity of the dorsoventral tuning gradient coexisted with discrete topography in the spatial scale of simultaneously recorded grid Cells. Conclusions The findings point to dorsoventral gradients as a fundamental property of entorhinal circuits, upon which modular organization may be expressed in select subpopulations.
James J. Knierim - One of the best experts on this subject based on the ideXlab platform.
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attractor dynamics of spatially correlated neural activity in the limbic system
Annual Review of Neuroscience, 2012Co-Authors: James J. Knierim, Kechen ZhangAbstract:Attractor networks are a popular computational construct used to model different brain systems. These networks allow elegant computations that are thought to represent a number of aspects of brain function. Although there is good reason to believe that the brain displays attractor dynamics, it has proven difficult to test experimentally whether any particular attractor architecture resides in any particular brain circuit. We review models and experimental evidence for three systems in the rat brain that are presumed to be components of the rat's navigational and memory system. Head-Direction Cells have been modeled as a ring attractor, grid Cells as a plane attractor, and place Cells both as a plane attractor and as a point attractor. Whereas the models have proven to be extremely useful conceptual tools, the experimental evidence in their favor, although intriguing, is still mostly circumstantial.
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cohesiveness of spatial and Directional representations recorded from neural ensembles in the anterior thalamus parasubiculum medial entorhinal cortex and hippocampus
Hippocampus, 2007Co-Authors: Eric L Hargreaves, D Yoganarasimha, James J. KnierimAbstract:Anatomical and physiological evidence suggests that hippo- campal place Cells derive their spatial firing properties from the medial entorhinal cortex (MEC) and other parahippocampal areas that send spatial and Directional input to the MEC. MEC neurons fire in a precise, geometric pattern, forming a hexagonal grid that tessellates the surface of environ- ments. Similar to place Cells and Head Direction Cells, the orientation of grid cell firing patterns can be controlled by visual landmarks, but the Cells maintain their firing patterns even in the dark. Place Cells and Head direc- tion Cells can also completely decouple from external landmarks in the light, but it is not known whether the MEC and parahippocampal regions exhibit similar properties or are more explicitly tied to external landmarks. We recorded neurons in the MEC, parasubiculum, and CA1 and Head direc- tion Cells of the anterior thalamus as the rat's internal Direction sense was pitted against a salient visual landmark by slowly rotating the rat in a cov- ered bucket while counter-rotating the visual cue. In different sessions, spa- tial firing rate maps and Head Direction tuning curves either rotated their preferred firing locations/Directions by the same amount as the bucket rotation or maintained their preferences in the external laboratory frame- work. In few cases, the firing preferences rotated with the cue card. When Cells from different regions were recorded simultaneously, the dominant response in one area almost always matched the response of the other areas. Although dominant responses were consistent throughout the re- cording regions, CA1 ensembles exhibited a greater degree of response het- erogeneity than other regions, which nearly all exhibited internally consist- ent responses. Thus, the parahippocampal and MEC input to the hippocam- pus can be controlled by the animal's internal Direction sense (presumably reflected in the firing of Head Direction Cells) and become completely decoupled from external sensory input, yet maintain internal coherence with each other and in general with the place cell system of the hippo- campus. V C 2007 Wiley-Liss, Inc.
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backward shift of Head Direction tuning curves of the anterior thalamus comparison with ca1 place fields
Neuron, 2006Co-Authors: D Yoganarasimha, James J. KnierimAbstract:The Head Direction cell system is composed of multiple regions associated with the hippocampal formation. The dynamics of Head Direction tuning curves (HDTCs) were compared with those of hippocampal place fields. In both familiar and cue-altered environments, as a rat ran an increasing number of laps on a track, the center of mass (COM) of the HDTC tended to shift backward, similar to shifting observed in place Cells. However, important differences existed between these Cells in terms of the shift patterns relative to the cue-altered conditions, the proportion of backward versus forward shifts, and the time course of shift resetting. The demonstration of backward COM shifts in Head Direction Cells and place Cells suggests that similar plasticity mechanisms (such as temporally asymmetric LTP induction or spike timing-dependent plasticity) may be at work in both brain systems, and these processes may reflect a general mechanism for storing learned sequences of neural activity patterns.
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Head Direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations comparison with hippocampal place Cells
The Journal of Neuroscience, 2006Co-Authors: D Yoganarasimha, James J. KnierimAbstract:Place Cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the Head Direction cell system. The representation of a well explored environment by CA1 place Cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same Direction (Lee et al., 2004). The present study tests whether the Head Direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place Cells and Head Direction Cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place Cells in ∼75% of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the Head Direction cell ensembles revealing a split representation of Head Direction. Instead, in most of the mismatch sessions, the Head Direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the Head Direction Cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence.
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deciphering the hippocampal polyglot the hippocampus as a path integration system
The Journal of Experimental Biology, 1996Co-Authors: Bruce L Mcnaughton, Katalin M Gothard, William E Skaggs, James J. Knierim, Carol A Barnes, Jason L Gerrard, M W Jung, Hemant S Kudrimoti, Yulin Qin, M SusterAbstract:Hippocampal 'place' Cells and the Head-Direction Cells of the dorsal presubiculum and related neocortical and thalamic areas appear to be part of a preconfigured network that generates an abstract internal representation of two-dimensional space whose metric is self-motion. It appears that viewpoint-specific visual information (e.g. landmarks) becomes secondarily bound to this structure by associative learning. These associations between landmarks and the preconfigured path integrator serve to set the origin for path integration and to correct for cumulative error. In the absence of familiar landmarks, or in darkness without a prior spatial reference, the system appears to adopt an initial reference for path integration independently of external cues. A hypothesis of how the path integration system may operate at the neuronal level is proposed.
Bruce L Mcnaughton - One of the best experts on this subject based on the ideXlab platform.
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spatial representation in the hippocampal formation a history
Nature Neuroscience, 2017Co-Authors: Edvard I. Moser, Bruce L McnaughtonAbstract:Since the first place cell was recorded and the cognitive-map theory was subsequently formulated, investigation of spatial representation in the hippocampal formation has evolved in stages. Early studies sought to verify the spatial nature of place cell activity and determine its sensory origin. A new epoch started with the discovery of Head Direction Cells and the realization of the importance of angular and linear movement-integration in generating spatial maps. A third epoch began when investigators turned their attention to the entorhinal cortex, which led to the discovery of grid Cells and border Cells. This review will show how ideas about integration of self-motion cues have shaped our understanding of spatial representation in hippocampal-entorhinal systems from the 1970s until today. It is now possible to investigate how specialized cell types of these systems work together, and spatial mapping may become one of the first cognitive functions to be understood in mechanistic detail.
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conjunctive representation of position Direction and velocity in entorhinal cortex
Science, 2006Co-Authors: Francesca Sargolini, Maybritt Moser, Bruce L Mcnaughton, Marianne Fyhn, Torkel Hafting, Menno P Witter, Edvard I. MoserAbstract:Grid Cells in the medial entorhinal cortex (MEC) are part of an environment-independent spatial coordinate system. To determine how information about location, Direction, and distance is integrated in the grid-cell network, we recorded from each principal cell layer of MEC in rats that explored two-dimensional environments. Whereas layer II was predominated by grid Cells, grid Cells colocalized with Head-Direction Cells and conjunctive grid x Head-Direction Cells in the deeper layers. All cell types were modulated by running speed. The conjunction of positional, Directional, and translational information in a single MEC cell type may enable grid coordinates to be updated during self-motion-based navigation.
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deciphering the hippocampal polyglot the hippocampus as a path integration system
The Journal of Experimental Biology, 1996Co-Authors: Bruce L Mcnaughton, Katalin M Gothard, William E Skaggs, James J. Knierim, Carol A Barnes, Jason L Gerrard, M W Jung, Hemant S Kudrimoti, Yulin Qin, M SusterAbstract:Hippocampal 'place' Cells and the Head-Direction Cells of the dorsal presubiculum and related neocortical and thalamic areas appear to be part of a preconfigured network that generates an abstract internal representation of two-dimensional space whose metric is self-motion. It appears that viewpoint-specific visual information (e.g. landmarks) becomes secondarily bound to this structure by associative learning. These associations between landmarks and the preconfigured path integrator serve to set the origin for path integration and to correct for cumulative error. In the absence of familiar landmarks, or in darkness without a prior spatial reference, the system appears to adopt an initial reference for path integration independently of external cues. A hypothesis of how the path integration system may operate at the neuronal level is proposed.
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Head Direction Cells in the rat posterior cortex i anatomical distribution and behavioral modulation
Experimental Brain Research, 1994Co-Authors: Longtang L Chen, Carol A Barnes, Lie Huey Lin, Edward J Green, Bruce L McnaughtonAbstract:We examined the behavioral modulation of Head-Directional information processing in neurons of the rat posterior cortices, including the medial prestriate (area Oc2M) and retrosplenial cortex (areas RSA and RSG). Single neurons were recorded in freely moving rats which were trained to perform a spatial working memory task on a radial-arm maze in a cue-controlled room. A dual-light-emitting diode (dual-LED) recording Headstage, mounted on the animals' Heads, was used to track Head position and orientation. Planar modes of motion, such as turns, straight motion, and nonlocomotive states, were categorized using an objective scheme based upon the differential contributions of movement parameters, including linear and angular velocity of the Head. Of 662 neurons recorded from the posterior cortices, 41 Head-Direction (HD) Cells were identified based on the criterion of maintained Directional bias in the absence of visual cues or in the dark. HD Cells constituted 7 of 257 (2.7%) Cells recorded in Oc2M, 26 of 311 (8.4%) Cells in RSA, and 8 of 94 (8.5%) Cells in RSG. Spatial tuning of HD cell firing was modulated by the animal's behaviors in some neurons. The behavioral modulation occurred either at the preferred Direction or at all Directions. Moreover, the behavioral selectivity was more robust for turns than straight motions, suggesting that the angular movements may significantly contribute to the Head-Directional processing. These behaviorally selective HD Cells were observed most frequently in Oc2M (4/7, 57%), as only 5 of 26 (19%) of RSA Cells and none of the RSG Cells showed behavioral modulation. These data, taken together with the anatomical evidence for a cascade of projections from Oc2M to RSA and thence to RSG, suggest that there may be a simple association between movement and Head-Directionality that serves to transform the egocentric movement representation in the neocortex into an allocentric Directional representation in the periallocortex.
Neil Burgess - One of the best experts on this subject based on the ideXlab platform.
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space in the brain how the hippocampal formation supports spatial cognition
Philosophical Transactions of the Royal Society B, 2014Co-Authors: Tom Hartley, Neil Burgess, Colin Lever, John OkeefeAbstract:Over the past four decades, research has revealed that Cells in the hippocampal formation provide an exquisitely detailed representation of an animal's current location and Heading. These findings have provided the foundations for a growing understanding of the mechanisms of spatial cognition in mammals, including humans. We describe the key properties of the major categories of spatial Cells: place Cells, Head Direction Cells, grid Cells and boundary Cells, each of which has a characteristic firing pattern that encodes spatial parameters relating to the animal's current position and orientation. These properties also include the theta oscillation, which appears to play a functional role in the representation and processing of spatial information. Reviewing recent work, we identify some themes of current research and introduce approaches to computational modelling that have helped to bridge the different levels of description at which these mechanisms have been investigated. These range from the level of molecular biology and genetics to the behaviour and brain activity of entire organisms. We argue that the neuroscience of spatial cognition is emerging as an exceptionally integrative field which provides an ideal test-bed for theories linking neural coding, learning, memory and cognition.
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Dual phase and rate coding in hippocampal place Cells: Theoretical significance and relationship to entorhinal grid Cells
Hippocampus, 2005Co-Authors: John O'keefe, Neil BurgessAbstract:We review the ideas and data behind the hypothesis that hippocampal pyramidal Cells encode information by their phase of firing relative to the theta rhythm of the EEG. Particular focus is given to the further hypothesis that variations in firing rate can encode information independently from that encoded by firing phase. We discuss possible explanation of the phase-precession effect in terms of interference between two independent oscillatory influences on the pyramidal cell membrane potential, and the extent to which firing phase reflects internal dynamics or external (environmental) variables. Finally, we propose a model of the firing of the recently discovered "grid Cells" in entorhinal cortex as part of a path-integration system, in combination with place Cells and Head-Direction Cells.
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dual phase and rate coding in hippocampal place Cells theoretical significance and relationship to entorhinal grid Cells
Hippocampus, 2005Co-Authors: John Okeefe, Neil BurgessAbstract:We review the ideas and data behind the hypothesis that hippocampal pyramidal Cells encode information by their phase of firing relative to the theta rhythm of the EEG. Particular focus is given to the further hypothesis that variations in firing rate can encode information independently from that encoded by firing phase. We discuss possible explanation of the phase-precession effect in terms of interference between two independent oscillatory influences on the pyramidal cell membrane potential, and the extent to which firing phase reflects inter- nal dynamics or external (environmental) variables. Finally, we propose a model of the firing of the recently discovered ''grid Cells'' in entorhi- nal cortex as part of a path-integration system, in combination with place Cells and Head-Direction Cells. V C 2005 Wiley-Liss, Inc.
