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Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior.

Haggerty DC, Ji D - Elife (2015)

Bottom Line: The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations.The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior.These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, United States.

ABSTRACT
Visual cues exert a powerful control over hippocampal place cell activities that encode external spaces. The functional interaction of visual cortical neurons and hippocampal place cells during spatial navigation behavior has yet to be elucidated. Here we show that, like hippocampal place cells, many neurons in the primary visual cortex (V1) of freely moving rats selectively fire at specific locations as animals run repeatedly on a track. The V1 location-specific activity leads hippocampal place cell activity both spatially and temporally. The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations. The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior. These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

No MeSH data available.


Illustration of overlapping, non-overlapping, and non-responsive V1-CA1 cell pairs.(A) An overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially overlapping firing fields (with 50–100% overlap). (B) A non-overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially non-overlapping firing fields. (C) A non-responsive pair: a non-location-responsive V1 cell (top) and a CA1 place cell (bottom). Boxed areas: the spatial intervals for probing the co-fluctuation of a given pair. For overlapping pair (A) and non-overlapping pairs (B), the spatial intervals were their firing fields. For Non-responsive pairs (C), the spatial interval for the location-responsive cell was its firing field, whereas for the non-location-responsive cell it was the location-responsive cell's firing field shifted with a small random distance that yielded a random overlap of 50–100% with the firing field of the other cell. The same V1 cell and CA1 place cell can be involved in multiple pairs. In this example the same CA1 place cell appeared in 3 pairs.DOI:http://dx.doi.org/10.7554/eLife.08902.010
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fig6s2: Illustration of overlapping, non-overlapping, and non-responsive V1-CA1 cell pairs.(A) An overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially overlapping firing fields (with 50–100% overlap). (B) A non-overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially non-overlapping firing fields. (C) A non-responsive pair: a non-location-responsive V1 cell (top) and a CA1 place cell (bottom). Boxed areas: the spatial intervals for probing the co-fluctuation of a given pair. For overlapping pair (A) and non-overlapping pairs (B), the spatial intervals were their firing fields. For Non-responsive pairs (C), the spatial interval for the location-responsive cell was its firing field, whereas for the non-location-responsive cell it was the location-responsive cell's firing field shifted with a small random distance that yielded a random overlap of 50–100% with the firing field of the other cell. The same V1 cell and CA1 place cell can be involved in multiple pairs. In this example the same CA1 place cell appeared in 3 pairs.DOI:http://dx.doi.org/10.7554/eLife.08902.010

Mentions: We also performed the same analysis on two control groups of V1-CA1 cell pairs (see Figure 6—figure supplement 2 for examples of V1-CA1 pairs). The first group consisted of 6681 pairs, each made of a CA1 place cell and a V1 location-responsive cell that both exhibited firing fields on a trajectory, but that their firing fields were non-overlapping. In this case, the Δrate and ΔCOM were computed within their most dominant firing fields on the trajectory. This control group, referred to as ‘non-overlapping pairs’, allowed us to test whether the CA1-V1 co-fluctuation was spatially confined within the overlapped firing fields. The second group contained 238 pairs, each composed of a CA1 cell that had place field on a trajectory and an active V1 cell that was not location-responsive on the trajectory. In this case, the Δrate and ΔCOM fluctuations of the V1 cell were computed within a spatial interval that was overlapped with the dominant CA1 place field (see ‘Materials and methods’). We call this group ‘non-responsive’ pairs, which allowed us to test whether the co-fluctuation was specific to the location-responsive V1 and CA1 cells. We found that the overlapping pairs had significantly higher correlation in Δrate than both non-overlapping (correlation: 0.062 ± 0.003; p < 0.0001, t-test) and non-responsive pairs (−0.023 ± 0.015; p < 0.0001; Figure 6D). Similarly, the overlapping pairs had significantly higher correlation in ΔCOM than non-overlapping (correlation: 0.0005 ± 0.0028; p < 0.0001) and non-responsive pairs (correlation: 0.047 ± 0.020; p < 0.0001; Figure 6D). We also computed the Δrate and ΔCOM correlations for CA1-CA1 cell pairs and for V1-V1 cell pairs. The results were similar: Overlapping pairs within each of the two brain areas were significantly correlated in both Δrate and ΔCOM and had significantly higher correlation than non-overlapping pairs and non-responsive pairs (Figure 6—figure supplement 3). Taken together, the results above demonstrate a specific, precise co-fluctuation in the firing rates and COMs of V1 location-responsive cells and CA1 place cells with overlapping firing fields, suggesting a functional interaction between these cells. Remarkably, this long–range interaction between cells in the distal V1 and CA1 was qualitatively similar to the local interaction within CA1 place cells.


Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior.

Haggerty DC, Ji D - Elife (2015)

Illustration of overlapping, non-overlapping, and non-responsive V1-CA1 cell pairs.(A) An overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially overlapping firing fields (with 50–100% overlap). (B) A non-overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially non-overlapping firing fields. (C) A non-responsive pair: a non-location-responsive V1 cell (top) and a CA1 place cell (bottom). Boxed areas: the spatial intervals for probing the co-fluctuation of a given pair. For overlapping pair (A) and non-overlapping pairs (B), the spatial intervals were their firing fields. For Non-responsive pairs (C), the spatial interval for the location-responsive cell was its firing field, whereas for the non-location-responsive cell it was the location-responsive cell's firing field shifted with a small random distance that yielded a random overlap of 50–100% with the firing field of the other cell. The same V1 cell and CA1 place cell can be involved in multiple pairs. In this example the same CA1 place cell appeared in 3 pairs.DOI:http://dx.doi.org/10.7554/eLife.08902.010
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Related In: Results  -  Collection

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fig6s2: Illustration of overlapping, non-overlapping, and non-responsive V1-CA1 cell pairs.(A) An overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially overlapping firing fields (with 50–100% overlap). (B) A non-overlapping pair: a location-responsive V1 cell (top) and a CA1 place cell (bottom) with spatially non-overlapping firing fields. (C) A non-responsive pair: a non-location-responsive V1 cell (top) and a CA1 place cell (bottom). Boxed areas: the spatial intervals for probing the co-fluctuation of a given pair. For overlapping pair (A) and non-overlapping pairs (B), the spatial intervals were their firing fields. For Non-responsive pairs (C), the spatial interval for the location-responsive cell was its firing field, whereas for the non-location-responsive cell it was the location-responsive cell's firing field shifted with a small random distance that yielded a random overlap of 50–100% with the firing field of the other cell. The same V1 cell and CA1 place cell can be involved in multiple pairs. In this example the same CA1 place cell appeared in 3 pairs.DOI:http://dx.doi.org/10.7554/eLife.08902.010
Mentions: We also performed the same analysis on two control groups of V1-CA1 cell pairs (see Figure 6—figure supplement 2 for examples of V1-CA1 pairs). The first group consisted of 6681 pairs, each made of a CA1 place cell and a V1 location-responsive cell that both exhibited firing fields on a trajectory, but that their firing fields were non-overlapping. In this case, the Δrate and ΔCOM were computed within their most dominant firing fields on the trajectory. This control group, referred to as ‘non-overlapping pairs’, allowed us to test whether the CA1-V1 co-fluctuation was spatially confined within the overlapped firing fields. The second group contained 238 pairs, each composed of a CA1 cell that had place field on a trajectory and an active V1 cell that was not location-responsive on the trajectory. In this case, the Δrate and ΔCOM fluctuations of the V1 cell were computed within a spatial interval that was overlapped with the dominant CA1 place field (see ‘Materials and methods’). We call this group ‘non-responsive’ pairs, which allowed us to test whether the co-fluctuation was specific to the location-responsive V1 and CA1 cells. We found that the overlapping pairs had significantly higher correlation in Δrate than both non-overlapping (correlation: 0.062 ± 0.003; p < 0.0001, t-test) and non-responsive pairs (−0.023 ± 0.015; p < 0.0001; Figure 6D). Similarly, the overlapping pairs had significantly higher correlation in ΔCOM than non-overlapping (correlation: 0.0005 ± 0.0028; p < 0.0001) and non-responsive pairs (correlation: 0.047 ± 0.020; p < 0.0001; Figure 6D). We also computed the Δrate and ΔCOM correlations for CA1-CA1 cell pairs and for V1-V1 cell pairs. The results were similar: Overlapping pairs within each of the two brain areas were significantly correlated in both Δrate and ΔCOM and had significantly higher correlation than non-overlapping pairs and non-responsive pairs (Figure 6—figure supplement 3). Taken together, the results above demonstrate a specific, precise co-fluctuation in the firing rates and COMs of V1 location-responsive cells and CA1 place cells with overlapping firing fields, suggesting a functional interaction between these cells. Remarkably, this long–range interaction between cells in the distal V1 and CA1 was qualitatively similar to the local interaction within CA1 place cells.

Bottom Line: The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations.The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior.These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, United States.

ABSTRACT
Visual cues exert a powerful control over hippocampal place cell activities that encode external spaces. The functional interaction of visual cortical neurons and hippocampal place cells during spatial navigation behavior has yet to be elucidated. Here we show that, like hippocampal place cells, many neurons in the primary visual cortex (V1) of freely moving rats selectively fire at specific locations as animals run repeatedly on a track. The V1 location-specific activity leads hippocampal place cell activity both spatially and temporally. The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations. The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior. These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

No MeSH data available.