scholarly journals Place cell map genesis via competitive learning and conjunctive coding in the dentate gyrus

2019 ◽  
Author(s):  
Soyoun Kim ◽  
Dajung Jung ◽  
Sébastien Royer

AbstractPlace cells exhibit spatially selective firing fields and collectively map the continuum of positions in environments; how such network pattern develops with experience remains unclear. Here, we recorded putative granule (GC) and mossy (MC) cells from the dentate gyrus (DG) over 27 days as mice repetitively ran through a sequence of objects fixed onto a treadmill belt. We observed a progressive transformation of GC spatial representations, from a sparse encoding of object locations and periodic spatial intervals to increasingly more single, evenly dispersed place fields, while MCs showed little transformation and preferentially encoded object locations. A competitive learning model of the DG reproduced GC transformations via the progressive integration of landmark-vector cells and grid cell inputs and required MC-mediated feedforward inhibition to evenly distribute GC representations, suggesting that GCs progressively encode conjunctions of objects and spatial information via competitive learning, while MCs help homogenize GC spatial representations.

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Soyoun Kim ◽  
Dajung Jung ◽  
Sébastien Royer

Abstract Place cells exhibit spatially selective firing fields that collectively map the continuum of positions in environments; how such activity pattern develops with experience is largely unknown. Here, we record putative granule cells (GCs) and mossy cells (MCs) from the dentate gyrus (DG) over 27 days as mice repetitively run through a sequence of objects fixed onto a treadmill belt. We observe a progressive transformation of GC spatial representations, from a sparse encoding of object locations and spatial patterns to increasingly more single, evenly dispersed place fields, while MCs show little transformation and preferentially encode object locations. A competitive learning model of the DG reproduces GC transformations via the progressive integration of landmark-vector cells and spatial inputs and requires MC-mediated feedforward inhibition to evenly distribute GC representations, suggesting that GCs slowly encode conjunctions of objects and spatial information via competitive learning, while MCs help homogenize GC spatial representations.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hannah S Wirtshafter ◽  
Matthew A Wilson

The lateral septum (LS), which is innervated by the hippocampus, is known to represent spatial information. However, the details of place representation in the LS, and whether this place information is combined with reward signaling, remains unknown. We simultaneously recorded from rat CA1 and caudodorsal lateral septum in rat during a rewarded navigation task and compared spatial firing in the two areas. While LS place cells are less numerous than in hippocampus, they are similar to the hippocampus in field size and number of fields per cell, but with field shape and center distributions that are more skewed toward reward. Spike cross-correlations between the hippocampus and LS are greatest for cells that have reward-proximate place fields, suggesting a role for the LS in relaying task-relevant hippocampal spatial information to downstream areas, such as the VTA.


2018 ◽  
Author(s):  
Alon B. Baram ◽  
Timothy H. Muller ◽  
James C.R. Whittington ◽  
Timothy E.J. Behrens

AbstractIt is proposed that a cognitive map encoding the relationships between objects supports the ability to flexibly navigate the world. Place cells and grid cells provide evidence for such a map in a spatial context. Emerging evidence suggests analogous cells code for non-spatial information. Further, it has been shown that grid cells resemble the eigenvectors of the relationship between place cells and can be learnt from local inputs. Here we show that these locally-learnt eigenvectors contain not only local information but also global knowledge that can provide both distributions over future states as well as a global distance measure encoding approximate distances between every object in the world. By simply changing the weights in the grid cell population, it is possible to switch between computing these different measures. We demonstrate a simple algorithm can use these measures to globally navigate arbitrary topologies without searching more than one step ahead. We refer to this as intuitive planning.


2020 ◽  
Author(s):  
Sebnem Tuncdemir ◽  
Andres Grosmark ◽  
Gergely Turi ◽  
Amei Shank ◽  
John Bowler ◽  
...  

Abstract During exploration, animals form an internal map of an environment by combining information about specific sensory cues or landmarks with the animal’s motion through space, a process which critically depends on the mammalian hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal trisynaptic circuit where self-motion and sensory cue information are integrated, yet it remains unknown how neurons within the DG encode both cue related (“what”) and spatial (“where”) information during cognitive map formation. Using two photon calcium imaging in head fixed mice running on a treadmill, along with on-line sensory cue manipulation at specific track locations, we have identified robust sensory cue responses in DG granule cells largely independent of spatial location. Granule cell cue responses are stable for long periods of time, selective for the modality of the stimulus and accompanied by strong inhibition of the firing of other active neurons. At the same time, there is a smaller fraction of neurons whose firing is spatially tuned but insensitive to the presentation of nearby cues, similar to traditional place cells. These results demonstrate the existence of “cue cells” in addition to the better characterized “place cells” in the DG, an important heterogeneity that has been previously overlooked. We hypothesize that the observed diversity of representations within the granule cell population may support parallel processing of complementary sensory and spatial information and impact the role of the dentate gyrus in spatial navigation and episodic memory.


2020 ◽  
Author(s):  
Brianna Vandrey ◽  
James A. Ainge

AbstractEpisodic memory requires information about objects to be integrated into a spatial framework. Place cells in the hippocampus encode spatial representations of objects that could be generated through signalling from the entorhinal cortex. Projections from lateral and medial entorhinal cortex to the hippocampus terminate in distal and proximal CA1, respectively. We recorded place cells in distal and proximal CA1 as rats explored an environment that contained objects. Place cells in distal CA1 demonstrated higher measures of spatial tuning and expressed place fields closer to objects. Further, remapping to object displacement was modulated by place field proximity to objects in distal, but not proximal CA1. Finally, representations of previous object locations were more precise in distal CA1. Our data suggest that lateral entorhinal cortex inputs to the hippocampus support spatial representations that are more precise and responsive to objects in cue-rich environments. This is consistent with functional segregation in the entorhinal-hippocampal circuits underlying object-place memory.


2020 ◽  
Author(s):  
Sebnem N. Tuncdemir ◽  
Andres D. Grosmark ◽  
Gergely Turi ◽  
Amei Shank ◽  
Jack Bowler ◽  
...  

AbstractDuring exploration, animals form an internal map of an environment by combining information about specific sensory cues or landmarks with the animal’s motion through space, a process which critically depends on the mammalian hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal trisynaptic circuit where self-motion and sensory cue information are integrated, yet it remains unknown how neurons within the DG encode both cue related (“what”) and spatial (“where”) information during cognitive map formation. Using two photon calcium imaging in head fixed mice running on a treadmill, along with on-line sensory cue manipulation at specific track locations, we have identified robust sensory cue responses in DG granule cells largely independent of spatial location. Granule cell cue responses are stable for long periods of time, selective for the modality of the stimulus and accompanied by strong inhibition of the firing of other active neurons. At the same time, there is a smaller fraction of neurons whose firing is spatially tuned but insensitive to the presentation of nearby cues, similar to traditional place cells. These results demonstrate the existence of “cue cells” in addition to the better characterized “place cells” in the DG, an important heterogeneity that has been previously overlooked. We hypothesize that the observed diversity of representations within the granule cell population may support parallel processing of complementary sensory and spatial information and impact the role of the dentate gyrus in spatial navigation and episodic memory.


2018 ◽  
Author(s):  
Tristan Shuman ◽  
Daniel Aharoni ◽  
Denise J. Cai ◽  
Christopher R. Lee ◽  
Spyridon Chavlis ◽  
...  

AbstractTemporal lobe epilepsy causes significant cognitive deficits in both human patients and rodent models, yet the specific circuit mechanisms that alter cognitive processes remain unknown. There is dramatic and selective interneuron death and axonal reorganization within the hippocampus of both humans and animal models, but the functional consequences of these changes on information processing at the neuronal population level have not been well characterized. To examine spatial representations of epileptic and control mice, we developed a novel wire-free miniature microscope to allow for unconstrained behavior during in vivo calcium imaging of neuronal activity. We found that epileptic mice running on a linear track had severely impaired spatial processing in CA1 within a single session, as place cells were less precise and less stable, and population coding was impaired. Long-term stability of place cells was also compromised as place cells in epileptic mice were highly unstable across short time intervals and completely remapped across a week. Because of the large-scale reorganization of inhibitory circuits in epilepsy, we hypothesized that degraded spatial representations were caused by dysfunctional inhibition. To test this hypothesis, we examined the temporal dynamics of hippocampal interneurons using silicon probes to simultaneously record from CA1 and dentate gyrus during head-fixed virtual navigation. We found that epileptic mice had a profound reduction in theta coherence between the dentate gyrus and CA1 regions and altered interneuron synchronization. In particular, dentate interneurons of epileptic mice had altered phase preferences to ongoing theta oscillations, which decorrelated inhibitory population firing between CA1 and dentate gyrus. To assess the specific contribution of desynchronization on spatial coding, we built a CA1 network model to simulate hippocampal desynchronization. Critically, we found that desynchronized inputs reduced the information content and stability of CA1 neurons, consistent with the experimental data. Together, these results demonstrate that temporally precise intra-hippocampal communication is critical for forming the spatial code and that desynchronized firing of hippocampal neuronal populations contributes to poor spatial processing in epileptic mice.


2019 ◽  
Author(s):  
Marcus K. Benna ◽  
Stefano Fusi

The observation of place cells has suggested that the hippocampus plays a special role in encoding spatial information. However, place cell responses are modulated by several non-spatial variables, and reported to be rather unstable. Here we propose a memory model of the hippocampus that provides a novel interpretation of place cells consistent with these observations. We hypothesize that the hippocampus is a memory device that takes advantage of the correlations between sensory experiences to generate compressed representations of the episodes that are stored in memory. A simple neural network model that can efficiently compress information naturally produces place cells that are similar to those observed in experiments. It predicts that the activity of these cells is variable and that the fluctuations of the place fields encode information about the recent history of sensory experiences. Place cells may simply be a consequence of a memory compression process implemented in the hippocampus.Significance StatementNumerous studies on humans revealed the importance of the hippocampus in memory formation. The rodent literature instead focused on the spatial representations that are observed in navigation experiments. Here we propose a simple model of the hippocampus that reconciles the main findings of the human and rodent studies. The model assumes that the hippocampus is a memory system that generates compressed representations of sensory experiences using previously acquired knowledge about the statistics of the world. These experiences can then be memorized more efficiently. The sensory experiences during the exploration of an environment, when compressed by the hippocampus, lead naturally to spatial representations similar to those observed in rodent studies and to the emergence of place cells.


2012 ◽  
Vol 2 (1) ◽  
Author(s):  
Javier I. Cuneo ◽  
Nicolas H. Quiroz ◽  
Victoria I. Weisz ◽  
Pablo F. Argibay

2002 ◽  
Vol 5 (1) ◽  
pp. 3-26 ◽  
Author(s):  
Karen Emmorey ◽  
Barbara Tversky

Two studies investigated the ramifications of encoding spatial locations via signing space for perspective choice in American Sign Language. Deaf signers (“speakers”) described the location of one of two identical objects either to a present addressee or to a remote addressee via a video monitor. Unlike what has been found for English speakers, ASL signers did not adopt their addressee’s spatial perspective when describing locations in a jointly viewed present environment; rather, they produced spatial descriptions utilizing shared space in which classifier and deictic signs were articulated at locations in signing space that schematically mapped to both the speaker’s and addressee’s view of object locations within the (imagined) environment. When the speaker and addressee were not jointly viewing the environment, speakers either adopted their addressee’s perspective via referential shift (i.e. locations in signing space were described as if the speaker were the addressee) or speakers expressed locations from their own perspective by describing locations from their view of a map of the environment and the addressee’s position within that environment. The results highlight crucial distinctions between the nature of perspective choice in signed languages in which signing space is used to convey spatial information and spoken languages in which spatial information is conveyed by lexical spatial terms. English speakers predominantly reduce their addressee’s cognitive load by adopting their addressee’s perspective, whereas in ASL shared space can be used (there is no true addressee or speaker perspective) and in other contexts, reversing speaker perspective is common in ASL and does not increase the addressee’s cognitive load.


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