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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.


Related in: MedlinePlus

Overlapping V1-V1 and CA1-CA1 cell pairs displayed correlated lap-by-lap fluctuation in firing rate and COM within their firing fields.(A) Average correlation in ∆rate and ∆COM for pairs of V1 location-responsive cells with overlapping firing fields (Overlapping), pairs of V1 location-responsive cells with non-overlapping firing fields (Non-overlapping), and pairs made of one location-responsive V1 cell and one non-location-responsive V1 cell (Non-responsive). (B) Same as (A), but after the modulation by speed and head direction was removed. (C, D) Same as A and B, but for CA1-CA1 cell pairs. Number of V1-V1 pairs: N = 803 overlapping pairs; 953 non-overlapping pairs; 30 non-responsive pairs. Number of CA1-CA1 pairs: N = 1621 overlapping pairs; 11,273 non-overlapping pairs; 121 non-responsive pairs. *: p < 0.05; **: p < 0.01; ***: p < 0.001; ****: p < 0.0001; t-test.DOI:http://dx.doi.org/10.7554/eLife.08902.011
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fig6s3: Overlapping V1-V1 and CA1-CA1 cell pairs displayed correlated lap-by-lap fluctuation in firing rate and COM within their firing fields.(A) Average correlation in ∆rate and ∆COM for pairs of V1 location-responsive cells with overlapping firing fields (Overlapping), pairs of V1 location-responsive cells with non-overlapping firing fields (Non-overlapping), and pairs made of one location-responsive V1 cell and one non-location-responsive V1 cell (Non-responsive). (B) Same as (A), but after the modulation by speed and head direction was removed. (C, D) Same as A and B, but for CA1-CA1 cell pairs. Number of V1-V1 pairs: N = 803 overlapping pairs; 953 non-overlapping pairs; 30 non-responsive pairs. Number of CA1-CA1 pairs: N = 1621 overlapping pairs; 11,273 non-overlapping pairs; 121 non-responsive pairs. *: p < 0.05; **: p < 0.01; ***: p < 0.001; ****: p < 0.0001; t-test.DOI:http://dx.doi.org/10.7554/eLife.08902.011

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)

Overlapping V1-V1 and CA1-CA1 cell pairs displayed correlated lap-by-lap fluctuation in firing rate and COM within their firing fields.(A) Average correlation in ∆rate and ∆COM for pairs of V1 location-responsive cells with overlapping firing fields (Overlapping), pairs of V1 location-responsive cells with non-overlapping firing fields (Non-overlapping), and pairs made of one location-responsive V1 cell and one non-location-responsive V1 cell (Non-responsive). (B) Same as (A), but after the modulation by speed and head direction was removed. (C, D) Same as A and B, but for CA1-CA1 cell pairs. Number of V1-V1 pairs: N = 803 overlapping pairs; 953 non-overlapping pairs; 30 non-responsive pairs. Number of CA1-CA1 pairs: N = 1621 overlapping pairs; 11,273 non-overlapping pairs; 121 non-responsive pairs. *: p < 0.05; **: p < 0.01; ***: p < 0.001; ****: p < 0.0001; t-test.DOI:http://dx.doi.org/10.7554/eLife.08902.011
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Related In: Results  -  Collection

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fig6s3: Overlapping V1-V1 and CA1-CA1 cell pairs displayed correlated lap-by-lap fluctuation in firing rate and COM within their firing fields.(A) Average correlation in ∆rate and ∆COM for pairs of V1 location-responsive cells with overlapping firing fields (Overlapping), pairs of V1 location-responsive cells with non-overlapping firing fields (Non-overlapping), and pairs made of one location-responsive V1 cell and one non-location-responsive V1 cell (Non-responsive). (B) Same as (A), but after the modulation by speed and head direction was removed. (C, D) Same as A and B, but for CA1-CA1 cell pairs. Number of V1-V1 pairs: N = 803 overlapping pairs; 953 non-overlapping pairs; 30 non-responsive pairs. Number of CA1-CA1 pairs: N = 1621 overlapping pairs; 11,273 non-overlapping pairs; 121 non-responsive pairs. *: p < 0.05; **: p < 0.01; ***: p < 0.001; ****: p < 0.0001; t-test.DOI:http://dx.doi.org/10.7554/eLife.08902.011
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.


Related in: MedlinePlus