Self-Motion and the Hippocampal Spatial Metric

Terrazas, Alejandro; Krause, Michael; Lipa, P.; Gothard, Katalin M.; Barnes, Carol A.; McNaughton, Bruce L.

doi:10.1523/jneurosci.0693-05.2005

Cited by 198 publications

(191 citation statements)

References 43 publications

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“…By contrast, no species may need grids larger than a few meters because grid maps are likely to be local and fragmented in all realistic environments 98 . An important point to note, however, is that humans are obviously not locomoting during fMRI scanning, and this might influence the scale of the place fields during scanning, similar to what has been observed in rodents locomoting by train instead of walking themselves 99 . Studies in monkeys have also been limited for practical reasons: thus far these have involved head fixation 94 .…”

Section: Spatial Processing In Primatesmentioning

confidence: 89%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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The precise functional role of the hippocampus remains a topic of much debate. According to a dominant view, the dorsal/posterior hippocampus is implicated in memory and spatial navigation and the ventral/anterior hippocampus mediates anxietyrelated behaviours. However, this 'dichotomy view' may need revision. Gene expression studies demonstrate multiple functional domains along the hippocampal long axis, which often exhibit sharply demarcated borders. By contrast, anatomical studies and electrophysiological recordings in rodents suggest that the long-axis is organized along a gradient. Together, these observations suggest a model in which functional long-axis gradients are superimposed on discrete functional domains. This model provides a potential framework to explain and test the multiple functions ascribed to the hippocampus.The hippocampus is a medial temporal lobe structure critically involved in episodic memory and spatial navigation [1][2][3][4][5][6][7] . Its long, curved form is present across all mammalian orders and runs along a dorsal (septal) to ventral (temporal) axis in rodents, corresponding to a posteriorto-anterior axis in humans (FIG. 1a-b). The same basic intrinsic circuitry is maintained throughout the long axis and across species (FIG. 1c). Despite this conserved intrinsic circuitry, the dorsal and ventral portions have different connectivities with cortical and subcortical areas, and this has long posed a question as to whether the hippocampus is functionally uniform along this axis. Here we review cross-species data that show how the seemingly disparate functions ascribed to the hippocampus can be accommodated by a model in which different functional properties exist along the longitudinal axis.The severe memory impairment suffered by patient H.M. following bilateral hippocampal resection 1 led to intensive study 8 of patients and animal models with hippocampal damage, with an ensuing characterisation of hippocampal function in terms of declarative memory 2 , encompassing both episodic and semantic memory. At the same time, however, evidence emerged for a hippocampal role in spatial memory, based on the discovery of hippocampal 'place cells' 9,10 and the demonstration that hippocampal lesions impair spatial memory 4 . Both the declarative memory hypothesis 11 and the spatial mapping hypothesis 12 of hippocampal function proposed a unitary model in which the entire hippocampus is dedicated

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Section: Spatial Processing In Primatesmentioning

confidence: 89%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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“…Previous experiments have shown that the phase precession slope of place cells correlated with the size of its place field (7,19,28) so that the total phase precession is always about one full cycle, and that both the phase precession slope and field size increase along the septotemporal axis of the hippocampus (29). It has been suggested that phase precession can be produced by faster oscillating pyramidal cells than the LFP, and it has been shown that the phase-space relationship is speed-independent (2), but no mechanisms were provided.…”

Section: Speed-dependent Oscillation Of Place Cells Can Keep the Spikmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

253

321

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The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward (''phase precession'') over a full cycle as the animal crosses the cell's receptive field (''place field''). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase-distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase-distance invariance of hippocampal place cells.cell assembly ͉ interneurons ͉ phase locking ͉ phase precession ͉ oscillations W hile animals navigate in an environment, the hippocampal local field potential (LFP) is characterized by a highly regular oscillation (8-10 Hz). Principal cells in the hippocampus show place-specific firing by two criteria. First, the firing is tuned to a particular location (''place field''), showing a bellshaped tuning curve centered around its preferred location (1). Second, the timing of spikes within subsequent cycles systematically shifts forward (''phase precession''), Ϸ1 full cycle in total, as the rat runs through the place field of the neuron (2, 3) (see also Fig. 1 A and B). Both the firing rate and discharge phase within a cycle are correlated with the rat's position. However, how the rate change and -phase precession of spikes are related is poorly understood. The available experiments support both a rate-phase interdependence (4-6) and independence (7).Several explanations for the place-phase relationship were put forward (4)(5)(6)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). To confront these models, we examined the relationship among running speed, oscillation frequency of place cells and LFP , and timing of spikes within the cycle. We show that principal cells oscillate at a frequency faster than the simultaneously recorded LFP oscillation, and that this oscillation frequency depends on the rat's running speed. Together with the place-and speed-dependent oscillation frequencies of interneurons, the findings support the hypothesis that place coding results from coordinated network activity. We propose that the locomotion speed-dependent oscillation of place cell assemblies may underlie the mechanisms responsible for distance encoding in the hippocampus. ResultsWe recorded the firing patterns of pyramidal cells, interneurons, and the LFP from the CA1 pyramidal layer of rats as they ran on a U-shap...

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“…Interestingly, when some self-generated movement information is eliminated, e.g., by moving a rat passively in the environment, place fields are larger than when a rat is actively moving in the same environment [24]. Similarly, when the environment is rotated around a stationary rat, and thus only the movement of distal visual objects suggests movement, the spatial information content per spike of place cells is reduced by 50% [25]; i.e., an experiment similar to virtual reality, or the experience one can have when sitting in a stationary train, watching an adjacent departing train. Thus, altogether these experiments indicate that the ensemble of spatial information derived from different sensory modalities contributes to the selectivity of place cells firing, and that the highest selectivity is obtained when all sources of spatial information are coherent, as is normally the case in the real world.…”

Section: As the World Turns: A Neurobiological Perspectivementioning

confidence: 99%

As the world turns: Short-term human spatial memory in egocentric and allocentric coordinates

Lavenex

Lecci

Prêtre

et al. 2011

Behavioural Brain Research

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We aimed to determine whether human subjects' reliance on different sources of spatial information encoded in different frames of reference (i.e., egocentric versus allocentric) affects their performance, decision time and memory capacity in a short-term spatial memory task performed in the real world. Subjects were asked to play the Memory game (a.k.a. the Concentration game) without an opponent, in four different conditions that controlled for the subjects' reliance on egocentric and/or allocentric frames of reference for the elaboration of a spatial representation of the image locations enabling maximal efficiency. We report experimental data from young adult men and women, and describe a mathematical model to estimate human short-term spatial memory capacity. We found that short-term spatial memory capacity was greatest when an egocentric spatial frame of reference enabled subjects to encode and remember the image locations. However, when egocentric information was not reliable, short-term spatial memory capacity was greater and decision time shorter when an allocentric representation of the image locations with respect to distant objects in the surrounding environment was available, as compared to when only a spatial representation encoding the relationships between the individual images, independent of the surrounding environment, was available. Our findings thus further demonstrate that changes in viewpoint produced by the movement of images placed in front of a stationary subject is not equivalent to the movement of the subject around stationary images. We discuss possible limitations of classical neuropsychological and virtual reality experiments of spatial memory, which typically restrict the sensory information normally available to human subjects in the real world.

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Self-Motion and the Hippocampal Spatial Metric

Cited by 198 publications

References 43 publications

Functional organization of the hippocampal longitudinal axis

Functional organization of the hippocampal longitudinal axis

Hippocampal place cell assemblies are speed-controlled oscillators

As the world turns: Short-term human spatial memory in egocentric and allocentric coordinates

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