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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.


Pair-wise cross-correlation between V1 and CA1 cells.(A, B) Firing activity (lap-by-lap spike raster and average firing rate curve; see Figure 2 legend for details) of a pair of V1 (A) and CA1 (B) cells on a trajectory of the C-shaped track. (C) Normalized cross-correlogram of the two cells in A and B. *: peak time of the cross-correlogram. (D) Histogram of the peak times for all highly significantly correlated pairs of V1 and CA1 cells (see ‘Materials and methods’). Note the bias of peak times toward positive time lags. (E) Peak times of those highly correlated V1-CA1 pairs with both displaying prospetive firing (Pros pairs) and of those pairs with one displaying prospective while the other displaying retrospective firing (Mix pairs). Each dot is a pair.DOI:http://dx.doi.org/10.7554/eLife.08902.007
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fig5: Pair-wise cross-correlation between V1 and CA1 cells.(A, B) Firing activity (lap-by-lap spike raster and average firing rate curve; see Figure 2 legend for details) of a pair of V1 (A) and CA1 (B) cells on a trajectory of the C-shaped track. (C) Normalized cross-correlogram of the two cells in A and B. *: peak time of the cross-correlogram. (D) Histogram of the peak times for all highly significantly correlated pairs of V1 and CA1 cells (see ‘Materials and methods’). Note the bias of peak times toward positive time lags. (E) Peak times of those highly correlated V1-CA1 pairs with both displaying prospetive firing (Pros pairs) and of those pairs with one displaying prospective while the other displaying retrospective firing (Mix pairs). Each dot is a pair.DOI:http://dx.doi.org/10.7554/eLife.08902.007

Mentions: We then analyzed the pair-wise cross-correlation between V1 location-responsive cells and CA1 place cells in the time domain. We used a normalized spike count cross-correlation (see ‘Materials and methods’), which is insensitive to the cells' firing rates, to quantify how the spiking activities of two cells were temporally correlated. Figure 5A–C shows an example pair of V1 and CA1 cells with both having well-defined firing fields on the same trajectory, which led to a prominent peak in its normalized cross-correlogram. The peak time quantified the temporal relationship of the two cells. For individual pairs of cells, this peak, especially that with a long peak time, might just passively reflect the fact that they had firing fields on the same trajectory, not necessarily reflecting any functional interaction. However, if a large number of such pairs are collected, the distribution of their peak times may inform the temporal relationship between the V1 and CA1 activities at the population level. Among 22,969 pairs of V1 location-responsive cells and CA1 place cells, we obtained 997 highly significantly correlated pairs (see ‘Materials and methods’ for definition) with peak correlation times within [−0.2, 0.2] s. The distribution of these peak times was significantly biased toward positive values (58% positive, 46% negative, p = 0.00017, binomial test; Figure 5D). The result indicates that, on average, V1 cells led CA1 cells in the time domain, suggesting the propagation of visual information from V1 to CA1. We also analyzed whether this direction of interaction was true to those V1-CA1 cell pairs with both showing bi-directional firing. Out of the 12 pairs with both the V1 and CA1 displaying prospective firing and 9 pairs with one displaying prospective firing while the other displaying retrospective firing (only 1 pair with both displaying retrospective firing), 9 (75%) and 6 (68%), respectively, showed positive peak times (Figure 5E), suggesting that the V1-CA1 interaction of these pairs followed the general trend at the population level.10.7554/eLife.08902.007Figure 5.Pair-wise cross-correlation between V1 and CA1 cells.


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

Haggerty DC, Ji D - Elife (2015)

Pair-wise cross-correlation between V1 and CA1 cells.(A, B) Firing activity (lap-by-lap spike raster and average firing rate curve; see Figure 2 legend for details) of a pair of V1 (A) and CA1 (B) cells on a trajectory of the C-shaped track. (C) Normalized cross-correlogram of the two cells in A and B. *: peak time of the cross-correlogram. (D) Histogram of the peak times for all highly significantly correlated pairs of V1 and CA1 cells (see ‘Materials and methods’). Note the bias of peak times toward positive time lags. (E) Peak times of those highly correlated V1-CA1 pairs with both displaying prospetive firing (Pros pairs) and of those pairs with one displaying prospective while the other displaying retrospective firing (Mix pairs). Each dot is a pair.DOI:http://dx.doi.org/10.7554/eLife.08902.007
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fig5: Pair-wise cross-correlation between V1 and CA1 cells.(A, B) Firing activity (lap-by-lap spike raster and average firing rate curve; see Figure 2 legend for details) of a pair of V1 (A) and CA1 (B) cells on a trajectory of the C-shaped track. (C) Normalized cross-correlogram of the two cells in A and B. *: peak time of the cross-correlogram. (D) Histogram of the peak times for all highly significantly correlated pairs of V1 and CA1 cells (see ‘Materials and methods’). Note the bias of peak times toward positive time lags. (E) Peak times of those highly correlated V1-CA1 pairs with both displaying prospetive firing (Pros pairs) and of those pairs with one displaying prospective while the other displaying retrospective firing (Mix pairs). Each dot is a pair.DOI:http://dx.doi.org/10.7554/eLife.08902.007
Mentions: We then analyzed the pair-wise cross-correlation between V1 location-responsive cells and CA1 place cells in the time domain. We used a normalized spike count cross-correlation (see ‘Materials and methods’), which is insensitive to the cells' firing rates, to quantify how the spiking activities of two cells were temporally correlated. Figure 5A–C shows an example pair of V1 and CA1 cells with both having well-defined firing fields on the same trajectory, which led to a prominent peak in its normalized cross-correlogram. The peak time quantified the temporal relationship of the two cells. For individual pairs of cells, this peak, especially that with a long peak time, might just passively reflect the fact that they had firing fields on the same trajectory, not necessarily reflecting any functional interaction. However, if a large number of such pairs are collected, the distribution of their peak times may inform the temporal relationship between the V1 and CA1 activities at the population level. Among 22,969 pairs of V1 location-responsive cells and CA1 place cells, we obtained 997 highly significantly correlated pairs (see ‘Materials and methods’ for definition) with peak correlation times within [−0.2, 0.2] s. The distribution of these peak times was significantly biased toward positive values (58% positive, 46% negative, p = 0.00017, binomial test; Figure 5D). The result indicates that, on average, V1 cells led CA1 cells in the time domain, suggesting the propagation of visual information from V1 to CA1. We also analyzed whether this direction of interaction was true to those V1-CA1 cell pairs with both showing bi-directional firing. Out of the 12 pairs with both the V1 and CA1 displaying prospective firing and 9 pairs with one displaying prospective firing while the other displaying retrospective firing (only 1 pair with both displaying retrospective firing), 9 (75%) and 6 (68%), respectively, showed positive peak times (Figure 5E), suggesting that the V1-CA1 interaction of these pairs followed the general trend at the population level.10.7554/eLife.08902.007Figure 5.Pair-wise cross-correlation between V1 and CA1 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.