Faculty Opinions recommendation of Specific evidence of low-dimensional continuous attractor dynamics in grid cells.

Author(s):  
Nachum Ulanovsky ◽  
Dori Derdikman
eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Haggai Agmon ◽  
Yoram Burak

The representation of position in the mammalian brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here, we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. In addition, our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.


2013 ◽  
Vol 16 (8) ◽  
pp. 1077-1084 ◽  
Author(s):  
KiJung Yoon ◽  
Michael A Buice ◽  
Caswell Barry ◽  
Robin Hayman ◽  
Neil Burgess ◽  
...  

2020 ◽  
Author(s):  
Haggai Agmon ◽  
Yoram Burak

ABSTRACTThe representation of position in the brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. We then show that our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.


2019 ◽  
Author(s):  
Diogo Santos-Pata ◽  
Riccardo Zucca ◽  
Héctor López-Carral ◽  
Paul F. M. J. Verschure

AbstractThe hexagonal tessellation pattern of grid cells scales up progressively along the dorsal-to-ventral axis of the medial entorhinal cortex (MEC) layer II. This scaling gradient has been hypothesized to originate either from inter population synaptic dynamics as postulated by attractor networks, from projected theta frequencies to different axis levels, as in oscillatory models, or from cellular dynamics dependent on hyperpolarization-activated cation currents. To test the hypothesis that intrinsic cellular properties account for the scale gradient as well as the different oscillatory frequencies observed along the dorsal-to-ventral axis, we have modeled and analyzed data from a population of grid cells simulated with spiking neurons interacting through low-dimensional attractor dynamics. To investigate the causal relationship between oscillatory frequencies and grid scale increase, we analyzed the dominant frequencies of the membrane potential for cells with distinct after-spike dynamics. We observed that intrinsic neuronal membrane properties of simulated cells could induce an increase of grid scale when modulated by after-spike reset values. Differences in the membrane potential oscillatory frequency were observed along the simulated dorsal-to-ventral axis, suggesting that, rather than driving to the increase of grid scale as proposed by interference models of grid cells, they are the result of intrinsic cellular properties of neurons at each axis level. Overall, our results suggest that the after-spike dynamics of cation currents may play a major role in determining the grid cells’ scale and that oscillatory frequencies are a consequence of intrinsic cellular properties that are specific to different levels of the dorsal-to-ventral axis in the MEC layer II.


2019 ◽  
Author(s):  
William de Cothi ◽  
Caswell Barry

AbstractThe hippocampus has long been observed to encode a representation of an animal’s position in space. Recent evidence suggests that the nature of this representation is somewhat predictive and can be modelled by learning a successor representation (SR) between distinct positions in an environment. However, this discretisation of space is subjective making it difficult to formulate predictions about how some environmental manipulations should impact the hippocampal representation. Here we present a model of place and grid cell firing as a consequence of learning a SR from a basis set of known neurobiological features – boundary vector cells (BVCs). The model describes place cell firing as the successor features of the SR, with grid cells forming a low-dimensional representation of these successor features. We show that the place and grid cells generated using the BVC-SR model provide a good account of biological data for a variety of environmental manipulations, including dimensional stretches, barrier insertions, and the influence of environmental geometry on the hippocampal representation of space.


2019 ◽  
Author(s):  
Davide Spalla ◽  
Alexis Dubreuil ◽  
Sophie Rosay ◽  
Remi Monasson ◽  
Alessandro Treves

The way grid cells represent space in the rodent brain has been a striking discovery, with theoret-ical implications still unclear. Differently from hippocampal place cells, which are known to encode multiple, environment-dependent spatial maps, grid cells have been widely believed to encode space through a single low dimensional manifold, in which coactivity relations between different neurons are preserved when the environment is changed. Does it have to be so? Here, we compute - using two alternative mathematical models - the storage capacity of a population of grid-like units, em-bedded in a continuous attractor neural network, for multiple spatial maps. We show that distinct representations of multiple environments can coexist, as existing models for grid cells have the po-tential to express several sets of hexagonal grid patterns, challenging the view of a universal grid map. This suggests that a population of grid cells can encode multiple non-congruent metric rela-tionships, a feature that could in principle allow a grid-like code to represent environments with a variety of different geometries and possibly conceptual and cognitive spaces, which may be expected to entail such context-dependent metric relationships.


2019 ◽  
Author(s):  
Rishidev Chaudhuri ◽  
Berk Gerçek ◽  
Biraj Pandey ◽  
Adrien Peyrache ◽  
Ila Fiete

AbstractThe brain constructs distributed representations of key low-dimensional variables. These variables may be external stimuli or internal constructs of quantities relevant for survival, such as a sense of one’s location in the world. We consider that the high-dimensional population-level activity vectors are the fundamental representational currency of a neural circuit, and these vectors trace out a low-dimensional manifold whose dimension and topology matches those of the represented variable. This manifold perspective — applied to the mammalian head direction circuit across rich waking behaviors and sleep — enables powerful inferences about circuit representation and mechanism, including: Direct visualization and blind discovery that the network represents a one-dimensional circular variable across waking and REM sleep; fully unsupervised decoding of the coded variable; stability and attractor dynamics in the representation; the discovery of new dynamical trajectories during sleep; the limiting role of external rather than internal noise in the fidelity of memory states; and the conclusion that the circuit is set up to integrate velocity inputs according to classical continuous attractor models.


2019 ◽  
Vol 31 (12) ◽  
pp. 2324-2347 ◽  
Author(s):  
Davide Spalla ◽  
Alexis Dubreuil ◽  
Sophie Rosay ◽  
Remi Monasson ◽  
Alessandro Treves

The way grid cells represent space in the rodent brain has been a striking discovery, with theoretical implications still unclear. Unlike hippocampal place cells, which are known to encode multiple, environment-dependent spatial maps, grid cells have been widely believed to encode space through a single low-dimensional manifold, in which coactivity relations between different neurons are preserved when the environment is changed. Does it have to be so? Here, we compute, using two alternative mathematical models, the storage capacity of a population of grid-like units, embedded in a continuous attractor neural network, for multiple spatial maps. We show that distinct representations of multiple environments can coexist, as existing models for grid cells have the potential to express several sets of hexagonal grid patterns, challenging the view of a universal grid map. This suggests that a population of grid cells can encode multiple noncongruent metric relationships, a feature that could in principle allow a grid-like code to represent environments with a variety of different geometries and possibly conceptual and cognitive spaces, which may be expected to entail such context-dependent metric relationships.


2019 ◽  
Author(s):  
Mirko Klukas ◽  
Marcus Lewis ◽  
Ila Fiete

AbstractWe shed light on the theoretical capabilities of entorhinal grid cells to encode variables of dimension greater than two. Our model constructs representations of high-dimensional inputs through a combination of low-dimensional random projections and “classical” low-dimensional hexagonal grid cell responses. Without reconfiguration of the recurrent circuit, the same system can flexibly encode multiple variables of different dimensions while maximizing the coding range (per dimension) by automatically trading-off dimension with an exponentially large coding range. In contrast to previously proposed schemes, the model does not require the formation of higher-dimensional grid responses, a cell-inefficient and rigid mechanism. The firing fields observed in flying bats or climbing rats can be generated by neurons that combine activity from multiple grid modules, each representing higher-dimensional spaces according to our model. The idea expands our understanding of grid cells, suggesting that they could implement a general circuit that generates on-demand coding and memory states for variables in high-dimensional vector spaces.


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