Parallel Processing of Sensory Cue and Spatial Information in the Dentate Gyrus

Parallel processing of sensory cue and spatial information in the Dentate Gyrus

10.21203/rs.3.rs-76845/v1 ◽

2020 ◽

Author(s):

Sebnem Tuncdemir ◽

Andres Grosmark ◽

Gergely Turi ◽

Amei Shank ◽

John Bowler ◽

...

Keyword(s):

Parallel Processing ◽

Dentate Gyrus ◽

Granule Cell ◽

Spatial Information ◽

Granule Cells ◽

Spatial Location ◽

Place Cells ◽

On Line ◽

Sensory Cue ◽

Self Motion

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.

Download Full-text

Parallel processing of sensory cue and spatial information in the Dentate Gyrus

10.1101/2020.02.13.947903 ◽

2020 ◽

Author(s):

Sebnem N. Tuncdemir ◽

Andres D. Grosmark ◽

Gergely Turi ◽

Amei Shank ◽

Jack Bowler ◽

...

Keyword(s):

Parallel Processing ◽

Dentate Gyrus ◽

Granule Cell ◽

Spatial Information ◽

Granule Cells ◽

Spatial Location ◽

Place Cells ◽

On Line ◽

Sensory Cue ◽

Self Motion

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.

Download Full-text

The computational influence of neurogenesis in the processing of spatial information in the dentate gyrus

Scientific Reports ◽

10.1038/srep00735 ◽

2012 ◽

Vol 2 (1) ◽

Cited By ~ 2

Author(s):

Javier I. Cuneo ◽

Nicolas H. Quiroz ◽

Victoria I. Weisz ◽

Pablo F. Argibay

Keyword(s):

Dentate Gyrus ◽

Spatial Information

Download Full-text

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

10.1101/748640 ◽

2019 ◽

Author(s):

Soyoun Kim ◽

Dajung Jung ◽

Sébastien Royer

Keyword(s):

Dentate Gyrus ◽

Spatial Information ◽

Grid Cell ◽

Place Cells ◽

Competitive Learning ◽

Spatial Representations ◽

Object Locations ◽

Network Pattern ◽

Treadmill Belt ◽

The Continuum

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.

Download Full-text

Adult-born neurons promote cognitive flexibility by improving memory precision and indexing

10.1101/2020.08.10.242966 ◽

2020 ◽

Author(s):

Gabriel Berdugo-Vega ◽

Chi-Chieh Lee ◽

Alexander Garthe ◽

Gerd Kempermann ◽

Federico Calegari

Keyword(s):

Stem Cells ◽

Dentate Gyrus ◽

Cognitive Flexibility ◽

Spatial Information ◽

Differential Regulation ◽

Memory Representations ◽

Adult Born Neurons ◽

Navigational Learning ◽

Memory Precision

SUMMARYThe dentate gyrus (DG) of the hippocampus is fundamental for cognitive flexibility and has the extraordinary ability to generate new neurons throughout life. Recent evidence suggested that adult-born neurons differentially modulate input to the DG during the processing of spatial information and novelty. However, how this differential regulation by neurogenesis is translated into different aspects contributing cognitive flexibility is unclear. Here, we increased adult-born neurons by a genetic expansion of neural stem cells and studied their influence during navigational learning. We found that increased neurogenesis improved memory precision, indexing and retention and that each of these gains was associated with a differential activation of specific DG compartments and better separation of memory representations in the DG-CA3 network. Our results highlight the role of adult-born neurons in promoting memory precision in the infrapyramidal and indexing in the suprapyramidal blade of the DG and together contributing to cognitive flexibility.One sentence summaryNeurogenesis improves memory precision and indexing.

Download Full-text

Binding experience-relevant neuronal assemblies through disinhibition

10.14293/s2199-1006.1.sor-.ppnyd9f.v1 ◽

2020 ◽

Author(s):

Raquel Garcia-Hernandez ◽

José María Caramés ◽

Elena Pérez-Montoyo ◽

Santiago Canals

Keyword(s):

Dentate Gyrus ◽

Spatial Information ◽

Granule Cells ◽

Moderate Increase ◽

The Novel ◽

Memory Encoding ◽

Neuronal Assemblies ◽

Inhibitory Tone ◽

Cell Inhibition ◽

Perisomatic Inhibition

Granule cells in the dentate gyrus (DGgc), a brain region important for spatial learning, are part of the engrams formed when an animal explores a new context. Previous work showed that modulation of DGgc activity by perisomatic inhibition bidirectionally regulates memory encoding. Whether this result is due to a differential recruitment of experience-relevant neuronal assemblies or the functional connectivity between them, is not yet known. We combined pharmacogenetic tools (DREADDs) to increase or decrease the activity of parvalbumin (PV)-interneurons in DG while mice encoded spatial information in the Novel Object Location task (NOL). Sixty min after memory encoding in the NOL task animals were sacrificed and their brains processed and quantified for c-Fos staining. Exploration in the NOL task induced a robust increase in the number of c-Fos+ cells across hippocampal subfields. However, the number of c-Fos+ cells, both in the hippocampus and extra-hippocampal structures like the medial prefrontal cortex (mPFC) and the nucleus accumbens, was constant regardless of the inhibitory tone in the DG. Only a moderate increase in c-Fos intensity per cell in DGgc was found in the PV-cell inhibition group. In contrast, we found a significant increase in the correlation between the number of c-Fos+ cells in all quantified neuronal assemblies during PV-inhibition, and a decrease during activation. Together, these data reveal a critical regulatory role of perisomatic inhibition in the dentate gyrus in binding experience-relevant neuronal assemblies in memory.

Download Full-text

Somatostatin-positive interneurons in the dentate gyrus of mice provide local- and long-range septal synaptic inhibition

eLife ◽

10.7554/elife.21105 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 28

Author(s):

Mei Yuan ◽

Thomas Meyer ◽

Christoph Benkowitz ◽

Shakuntala Savanthrapadian ◽

Laura Ansel-Bollepalli ◽

...

Keyword(s):

Dentate Gyrus ◽

Spatial Information ◽

Molecular Layer ◽

Activity Patterns ◽

Long Term Potentiation ◽

Medial Septum ◽

Perforant Path ◽

Term Potentiation ◽

Memory Acquisition

Somatostatin-expressing-interneurons (SOMIs) in the dentate gyrus (DG) control formation of granule cell (GC) assemblies during memory acquisition. Hilar-perforant-path-associated interneurons (HIPP cells) have been considered to be synonymous for DG-SOMIs. Deviating from this assumption, we show two functionally contrasting DG-SOMI-types. The classical feedback-inhibitory HIPPs distribute axon fibers in the molecular layer. They are engaged by converging GC-inputs and provide dendritic inhibition to the DG circuitry. In contrast, SOMIs with axon in the hilus, termed hilar interneurons (HILs), provide perisomatic inhibition onto GABAergic cells in the DG and project to the medial septum. Repetitive activation of glutamatergic inputs onto HIPP cells induces long-lasting-depression (LTD) of synaptic transmission but long-term-potentiation (LTP) of synaptic signals in HIL cells. Thus, LTD in HIPPs may assist flow of spatial information from the entorhinal cortex to the DG, whereas LTP in HILs may facilitate the temporal coordination of GCs with activity patterns governed by the medial septum.

Download Full-text