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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

Modulation of V1 and CA1 firing activities by speed and head direction.(A) Correlations between lap-by-lap speed and Δrate and between lap-by-lap speed and ΔCOM for example V1 and CA1 cells (the same as in Figure 6—figure supplement 1, panel B). Solid line: linear regression. R, P: Pearson's correlation and the associated p-value. Overall, speed was significantly correlated (p < 0.05) with Δrate in 25% (N = 107 out of 428) of V1 location-responsive cells and 41% (N = 619 out of 1510) of CA1 place cells, and with ΔCOM in 14% (N = 60) of V1 location-responsive cells and 25% (N = 378) of CA1 place cells. (B) Same as A, but between head direction fluctuation (Δhdir) and Δrate and between Δhdir and ΔCOM for the same V1 and CA1 cells in A. Δhdir was significantly correlated with Δrate in 12% (N = 51) of location-responsive V1 cells and in 21% (N = 317) of CA1 place cells, and with ΔCOM in 23% (N = 98) of location-responsive V1 cells and in 23% (N = 347) of CA1 place cells. (C) Distributions of speed-Δrate and speed-ΔCOM correlation values for all CA1 place cells and location-responsive V1 cells. Dashed lines: 0 correlation. The speed-Δrate distribution was skewed to the positive side for both V1 (0.064 ± 0.014; p < 0.0001, t-test compared with 0) and CA1 cells (0.16 ± 0.009, p < 0.0001), indicating that at the population level both V1 and CA1 cells increased their firing rates as speed increased. The speed-ΔCOM distribution was slightly but significantly skewed toward a positive mean for V1 (0.029 ± 0.011, p = 0.014), but not for CA1 cells (0.010 ± 0.008, p = 0.18), suggesting that, as speed increased, V1 cells' firing locations tended to move slightly forward along the animal's movement direction. (D) Same as (C), but for Δhdir-Δrate and Δhdir-ΔCOM distributions. The Δhdir–Δrate distribution was centered near 0 for both V1 (−0.0052 ± 0.011, p = 0.44) and CA1 (0.0057 ± 0.0073, p = 0.64) cells, indicating no systematic relationship between firing rate and head direction at the population level, even though each individual cell could increase or decrease firing rate as head direction was changed from left to right or vice versa. This result is expected if we assume that the V1 or CA1 cells as a group should not show any preferred head direction, even through individual V1 cells are tuned to particular directions. The Δhdir - ΔCOM distribution was similarly centered near 0 for both V1 (0.009 ± 0.015, p = 0.53) and CA1 (0.003 ± 0.008, p = 0.68) (right).DOI:http://dx.doi.org/10.7554/eLife.08902.012
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fig6s4: Modulation of V1 and CA1 firing activities by speed and head direction.(A) Correlations between lap-by-lap speed and Δrate and between lap-by-lap speed and ΔCOM for example V1 and CA1 cells (the same as in Figure 6—figure supplement 1, panel B). Solid line: linear regression. R, P: Pearson's correlation and the associated p-value. Overall, speed was significantly correlated (p < 0.05) with Δrate in 25% (N = 107 out of 428) of V1 location-responsive cells and 41% (N = 619 out of 1510) of CA1 place cells, and with ΔCOM in 14% (N = 60) of V1 location-responsive cells and 25% (N = 378) of CA1 place cells. (B) Same as A, but between head direction fluctuation (Δhdir) and Δrate and between Δhdir and ΔCOM for the same V1 and CA1 cells in A. Δhdir was significantly correlated with Δrate in 12% (N = 51) of location-responsive V1 cells and in 21% (N = 317) of CA1 place cells, and with ΔCOM in 23% (N = 98) of location-responsive V1 cells and in 23% (N = 347) of CA1 place cells. (C) Distributions of speed-Δrate and speed-ΔCOM correlation values for all CA1 place cells and location-responsive V1 cells. Dashed lines: 0 correlation. The speed-Δrate distribution was skewed to the positive side for both V1 (0.064 ± 0.014; p < 0.0001, t-test compared with 0) and CA1 cells (0.16 ± 0.009, p < 0.0001), indicating that at the population level both V1 and CA1 cells increased their firing rates as speed increased. The speed-ΔCOM distribution was slightly but significantly skewed toward a positive mean for V1 (0.029 ± 0.011, p = 0.014), but not for CA1 cells (0.010 ± 0.008, p = 0.18), suggesting that, as speed increased, V1 cells' firing locations tended to move slightly forward along the animal's movement direction. (D) Same as (C), but for Δhdir-Δrate and Δhdir-ΔCOM distributions. The Δhdir–Δrate distribution was centered near 0 for both V1 (−0.0052 ± 0.011, p = 0.44) and CA1 (0.0057 ± 0.0073, p = 0.64) cells, indicating no systematic relationship between firing rate and head direction at the population level, even though each individual cell could increase or decrease firing rate as head direction was changed from left to right or vice versa. This result is expected if we assume that the V1 or CA1 cells as a group should not show any preferred head direction, even through individual V1 cells are tuned to particular directions. The Δhdir - ΔCOM distribution was similarly centered near 0 for both V1 (0.009 ± 0.015, p = 0.53) and CA1 (0.003 ± 0.008, p = 0.68) (right).DOI:http://dx.doi.org/10.7554/eLife.08902.012

Mentions: Next, we examined whether the co-fluctuation of activity in overlapping V1-CA1 cell pairs could be explained by the lap-by-lap behavioral fluctuations. As expected (Huxter et al., 2003; Saleem et al., 2013), the firing rate and COM were modulated by speed and head direction in many V1 and CA1 cells (Figure 6—figure supplement 4). We quantified the modulation of both speed and head direction on Δrate/ΔCOM by a multi-variant linear regression and then removed the modulation to obtain the modified lap-by-lap fluctuations in firing rate/COM (modified Δrate/ΔCOM), which were no longer correlated with speed or head direction (see ‘Materials and methods’). We computed the correlations in the modified Δrate/ΔCOM for overlapping V1-CA1 cell pairs. For the pair in Figure 6A, the correlations in their modified Δrate and ΔCOM remained unchanged (Figure 6E), although there was a modest reduction in other pairs (Figure 6—figure supplement 1). For the group of overlapping V1-CA1 pairs, the average correlation between the modified Δrate (0.14 ± 0.009) remained significantly greater than 0 (p < 0.0001, t-test), and was significantly higher than those of non-overlapping (0.018 ± 0.002, p < 0.0001) and non-responsive (−0.019 ± 0.014, p < 0.0001) V1-CA1 pairs (Figure 6F). Similarly, the average correlation between the modified ΔCOM (0.13 ± 0.009) was also significantly greater than 0 (p < 0.0001), and was significantly higher than those of non-overlapping (−0.003 ± 0.003, p < 0.0001) and non-responsive (0.029 ± 0.018, p < 0.0001) V1-CA1 pairs (Figure 6F). From these results, we conclude that, behavioral variations cannot fully account for the correlation in the firing rate and COM of overlapping V1-CA1 cell pairs.


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

Haggerty DC, Ji D - Elife (2015)

Modulation of V1 and CA1 firing activities by speed and head direction.(A) Correlations between lap-by-lap speed and Δrate and between lap-by-lap speed and ΔCOM for example V1 and CA1 cells (the same as in Figure 6—figure supplement 1, panel B). Solid line: linear regression. R, P: Pearson's correlation and the associated p-value. Overall, speed was significantly correlated (p < 0.05) with Δrate in 25% (N = 107 out of 428) of V1 location-responsive cells and 41% (N = 619 out of 1510) of CA1 place cells, and with ΔCOM in 14% (N = 60) of V1 location-responsive cells and 25% (N = 378) of CA1 place cells. (B) Same as A, but between head direction fluctuation (Δhdir) and Δrate and between Δhdir and ΔCOM for the same V1 and CA1 cells in A. Δhdir was significantly correlated with Δrate in 12% (N = 51) of location-responsive V1 cells and in 21% (N = 317) of CA1 place cells, and with ΔCOM in 23% (N = 98) of location-responsive V1 cells and in 23% (N = 347) of CA1 place cells. (C) Distributions of speed-Δrate and speed-ΔCOM correlation values for all CA1 place cells and location-responsive V1 cells. Dashed lines: 0 correlation. The speed-Δrate distribution was skewed to the positive side for both V1 (0.064 ± 0.014; p < 0.0001, t-test compared with 0) and CA1 cells (0.16 ± 0.009, p < 0.0001), indicating that at the population level both V1 and CA1 cells increased their firing rates as speed increased. The speed-ΔCOM distribution was slightly but significantly skewed toward a positive mean for V1 (0.029 ± 0.011, p = 0.014), but not for CA1 cells (0.010 ± 0.008, p = 0.18), suggesting that, as speed increased, V1 cells' firing locations tended to move slightly forward along the animal's movement direction. (D) Same as (C), but for Δhdir-Δrate and Δhdir-ΔCOM distributions. The Δhdir–Δrate distribution was centered near 0 for both V1 (−0.0052 ± 0.011, p = 0.44) and CA1 (0.0057 ± 0.0073, p = 0.64) cells, indicating no systematic relationship between firing rate and head direction at the population level, even though each individual cell could increase or decrease firing rate as head direction was changed from left to right or vice versa. This result is expected if we assume that the V1 or CA1 cells as a group should not show any preferred head direction, even through individual V1 cells are tuned to particular directions. The Δhdir - ΔCOM distribution was similarly centered near 0 for both V1 (0.009 ± 0.015, p = 0.53) and CA1 (0.003 ± 0.008, p = 0.68) (right).DOI:http://dx.doi.org/10.7554/eLife.08902.012
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fig6s4: Modulation of V1 and CA1 firing activities by speed and head direction.(A) Correlations between lap-by-lap speed and Δrate and between lap-by-lap speed and ΔCOM for example V1 and CA1 cells (the same as in Figure 6—figure supplement 1, panel B). Solid line: linear regression. R, P: Pearson's correlation and the associated p-value. Overall, speed was significantly correlated (p < 0.05) with Δrate in 25% (N = 107 out of 428) of V1 location-responsive cells and 41% (N = 619 out of 1510) of CA1 place cells, and with ΔCOM in 14% (N = 60) of V1 location-responsive cells and 25% (N = 378) of CA1 place cells. (B) Same as A, but between head direction fluctuation (Δhdir) and Δrate and between Δhdir and ΔCOM for the same V1 and CA1 cells in A. Δhdir was significantly correlated with Δrate in 12% (N = 51) of location-responsive V1 cells and in 21% (N = 317) of CA1 place cells, and with ΔCOM in 23% (N = 98) of location-responsive V1 cells and in 23% (N = 347) of CA1 place cells. (C) Distributions of speed-Δrate and speed-ΔCOM correlation values for all CA1 place cells and location-responsive V1 cells. Dashed lines: 0 correlation. The speed-Δrate distribution was skewed to the positive side for both V1 (0.064 ± 0.014; p < 0.0001, t-test compared with 0) and CA1 cells (0.16 ± 0.009, p < 0.0001), indicating that at the population level both V1 and CA1 cells increased their firing rates as speed increased. The speed-ΔCOM distribution was slightly but significantly skewed toward a positive mean for V1 (0.029 ± 0.011, p = 0.014), but not for CA1 cells (0.010 ± 0.008, p = 0.18), suggesting that, as speed increased, V1 cells' firing locations tended to move slightly forward along the animal's movement direction. (D) Same as (C), but for Δhdir-Δrate and Δhdir-ΔCOM distributions. The Δhdir–Δrate distribution was centered near 0 for both V1 (−0.0052 ± 0.011, p = 0.44) and CA1 (0.0057 ± 0.0073, p = 0.64) cells, indicating no systematic relationship between firing rate and head direction at the population level, even though each individual cell could increase or decrease firing rate as head direction was changed from left to right or vice versa. This result is expected if we assume that the V1 or CA1 cells as a group should not show any preferred head direction, even through individual V1 cells are tuned to particular directions. The Δhdir - ΔCOM distribution was similarly centered near 0 for both V1 (0.009 ± 0.015, p = 0.53) and CA1 (0.003 ± 0.008, p = 0.68) (right).DOI:http://dx.doi.org/10.7554/eLife.08902.012
Mentions: Next, we examined whether the co-fluctuation of activity in overlapping V1-CA1 cell pairs could be explained by the lap-by-lap behavioral fluctuations. As expected (Huxter et al., 2003; Saleem et al., 2013), the firing rate and COM were modulated by speed and head direction in many V1 and CA1 cells (Figure 6—figure supplement 4). We quantified the modulation of both speed and head direction on Δrate/ΔCOM by a multi-variant linear regression and then removed the modulation to obtain the modified lap-by-lap fluctuations in firing rate/COM (modified Δrate/ΔCOM), which were no longer correlated with speed or head direction (see ‘Materials and methods’). We computed the correlations in the modified Δrate/ΔCOM for overlapping V1-CA1 cell pairs. For the pair in Figure 6A, the correlations in their modified Δrate and ΔCOM remained unchanged (Figure 6E), although there was a modest reduction in other pairs (Figure 6—figure supplement 1). For the group of overlapping V1-CA1 pairs, the average correlation between the modified Δrate (0.14 ± 0.009) remained significantly greater than 0 (p < 0.0001, t-test), and was significantly higher than those of non-overlapping (0.018 ± 0.002, p < 0.0001) and non-responsive (−0.019 ± 0.014, p < 0.0001) V1-CA1 pairs (Figure 6F). Similarly, the average correlation between the modified ΔCOM (0.13 ± 0.009) was also significantly greater than 0 (p < 0.0001), and was significantly higher than those of non-overlapping (−0.003 ± 0.003, p < 0.0001) and non-responsive (0.029 ± 0.018, p < 0.0001) V1-CA1 pairs (Figure 6F). From these results, we conclude that, behavioral variations cannot fully account for the correlation in the firing rate and COM of overlapping V1-CA1 cell pairs.

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