Models of spatial and temporal dimensions of memory

Hasselmo, Michael E.; Hinman, James R.; Dannenberg, Heinz; Stern, Chantal E.

doi:10.1016/j.cobeha.2017.05.024

Cited by 15 publications

(11 citation statements)

References 91 publications

(152 reference statements)

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“…The prevailing interpretation of these distortions has been that a rescaled environment induces a rescaled version of the cognitive map [10,12,14,16,18,22,29,37,39,41,45]. Our results suggest an alternative interpretation.…”

Section: Discussionmentioning

confidence: 49%

Environmental deformations dynamically shift the grid cell spatial metric

Keinath

Epstein

Balasubramanian

2017

Preprint

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2 SummaryWe propose a unified explanation for the diverse distortions in time-averaged activity of grid and place cells observed after environmental deformations. In our account, input from border cells resets the spatial phase but not the spatial scale of grid cells, maintaining learned relationships between grid phase and environmental boundaries. A computational model implementing this mechanism reproduced several commonly observed experimental effects, including scaledependent distortions in time-averaged grid fields after environmental deformation, and stretched, duplicated, and fractured place fields. Furthermore, this model predicted a striking new effect: dynamic, history-dependent 'shifts' in grid phase. We reanalyzed two classic datasets on grid rescaling and found clear evidence for such shifts, which have not previously been reported. These results invite a reconceptualization of the effects of environmental deformations on spatial representations -rather than rescaling the spatial metric of the cognitive map, as previously believed, alterations in environmental geometric may dynamically shift the map.. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/174367 doi: bioRxiv preprint first posted online Aug. 10, 2017; 3 The cognitive map is thought to be a metric representation of space that preserves distances between represented locations [1,2]. Entorhinal grid cells are hypothesized to generate this metric by maintaining an internally-generated, path-integrated representation of space [3][4][5][6][7][8]. Results of environmental deformation experiments have led to the belief that this metric is fundamentally malleable [9][10][11]. In these experiments, neural activity is recorded as a rat explores deformed versions of a familiar environment where chamber walls have been stretched, compressed, removed, or inserted. Such deformations induce a number of distortions in the time-averaged activity of both grid [9,11] and hippocampal place cells [12][13][14][15][16]. Often described as 'rescaling', these distortions have been taken to suggest that the spatial metric of the cognitive map can be reshaped by altering environmental geometry [9,17,18]. Crucially, however, this interpretation assumes that the distortions observed in the time-averaged rate maps of these cells directly reflect corresponding changes to the underlying spatial code. Here, we propose and test an alternative mechanism which challenges this interpretation and instead indicates that during environmental deformations the grid cell spatial metric does not rescale, but instead undergoes dynamical, history-dependent phase shifts.We hypothesize, as others have [10,[19][20][21][22][23], that border cells interact with grid cells in familiar environments to maintain learned relationships between grid phase and boundaries. Here we further propose that the same mechanism is responsible for inducing diverse and u...

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Section: Discussionmentioning

confidence: 49%

Environmental deformations dynamically shift the grid cell spatial metric

Keinath

Epstein

Balasubramanian

2017

Preprint

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“…Oscillatory interference models of path integration hypothesize that the slope of the theta frequency versus running speed correlation reflects the presence of velocity-controlled oscillators whose frequencies increase with running speed (Burgess, 2008). Computational models suggest a possible role of cholinergic modulation in coding of novelty, spatial location, and running speed in the entorhinal cortex (Hasselmo et al, 2017). The y-intercept of the theta frequency versus running speed relationship is affected by anxiolytic drugs (Wells et al, 2013;Monaghan et al, 2017), whereas environmental novelty (Wells et al, 2013) and muscarinic cholinergic signaling (Newman et al, 2013) have been shown to specifically affect the slope of the theta frequency to running speed relationship.…”

Section: Introductionmentioning

confidence: 99%

The firing rate speed code of entorhinal speed cells differs across behaviorally relevant time scales and does not depend on medial septum inputs

et al. 2019

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The firing rate of speed cells, a dedicated subpopulation of neurons in the medial entorhinal cortex (MEC), is correlated with running speed. This correlation has been interpreted as a speed code used in various computational models for path integration. These models consider firing rate to be linearly tuned by running speed in real-time. However, estimation of firing rates requires integration of spiking events over time, setting constraints on the temporal accuracy of the proposed speed code. We therefore tested whether the proposed speed code by firing rate is accurate at short time scales using data obtained from open-field recordings in male rats and mice. We applied a novel filtering approach differentiating between speed codes at multiple time scales ranging from deciseconds to minutes. In addition, we determined the optimal integration time window for firing-rate estimation using a general likelihood framework and calculated the integration time window that maximizes the correlation between firing rate and running speed. Data show that these time windows are on the order of seconds, setting constraints on real-time speed coding by firing rate. We further show that optogenetic inhibition of either cholinergic, GABAergic, or glutamatergic neurons in the medial septum/diagonal band of Broca does not affect modulation of firing rates by running speed at each time scale tested. These results are relevant for models of path integration and for our understanding of how behavioral activity states may modulate firing rates and likely information processing in the MEC.

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“…Recent neuroimaging experiments suggest that different aspects of complex scenes can be represented concurrently, such as the fine-grained information about the color of objects embedded within scenes (Richter et al, 2016). Moreover, fine-and coarse-grained detail about complex scenes are represented within the medial temporal lobes and prefrontal cortex (Cooper & Ritchey, 2019;Kolarik, Baer, Shahlaie, Yonelinas, & Ekstrom, 2018;Nilakantan, Bridge, VanHaerents, & Voss, 2018;Stevenson et al, 2018;Yonelinas, 2013), perhaps modulated by differences in the neural dynamics associated with fineand coarse-grained spatial information (Brunec, Moscovitch, & Barense, 2018;Bush, Barry, & Burgess, 2014;Collin, Millivojevic, & Doeller, 2015;Hasselmo et al, 2017;Poppenk, Evensmoen, Moscovitch, & Nadel, 2013). In one task, participants reconstructed the color, orientation, and spatial position associated with real-world objects studied on a 2D circle (Richter et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Visual interference can help and hinder memory: Capturing representational detail using the Validated Circular Shape Space

Liang

Lee

et al. 2019

Preprint

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Previous work suggests that the similarity of distracting information differentially alters how memories are forgotten. Though these effects have been shown for color memory, it is unclear if they extend to other modalities such as shape. In a first experiment, we created the Validated Circular Shape Space (VCS space), the first perceptually uniform "Shape Wheel" whereby subjective similarity was empirically quantified by angular distance on a 2D circle. In a second experiment, we utilized VCS space to examine the impact of distractor similarity on shape memory. A converging set of mixture model and model-free analyses revealed that distractor similarity differentially impacted memory detail. Dissimilar distractors disrupted both fine-and coarse-grained information, rendering the memory inaccessible. In contrast, similar distractors disrupted fine-grained but increased the reliance on coarse-grained information, rendering the memory blurred. As these effects were consistent across domains for both color and shape, we suggest these findings provide converging evidence for a set of general principles regarding how the nature of distracting information impacts memory. More generally, VCS space can be used to not only quantify subjective similarity but to also quantify memory fidelity for shape, a currently underexplored feature type in memory experiments.

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Models of spatial and temporal dimensions of memory

Cited by 15 publications

References 91 publications

Environmental deformations dynamically shift the grid cell spatial metric

Environmental deformations dynamically shift the grid cell spatial metric

The firing rate speed code of entorhinal speed cells differs across behaviorally relevant time scales and does not depend on medial septum inputs

Visual interference can help and hinder memory: Capturing representational detail using the Validated Circular Shape Space

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