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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

Experience dependence of V1 and CA1 firing activities on the C-shaped track.(A, B) Cumulative distributions of overall firing rate (A) and SMI (B) of active V1 and CA1 cells on different days (T1 – T3, see texts for definition). (C) The average (mean ± S.E.) correlation in the lap-by-lap Δrate (left) and ΔCOM (right) fluctuations for overlapping V1-CA1 cell pairs on different days. (D) Same as C, but for the correlation in modified Δrate and ΔCOM after removing the modulation by speed and head direction.DOI:http://dx.doi.org/10.7554/eLife.08902.015
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fig7: Experience dependence of V1 and CA1 firing activities on the C-shaped track.(A, B) Cumulative distributions of overall firing rate (A) and SMI (B) of active V1 and CA1 cells on different days (T1 – T3, see texts for definition). (C) The average (mean ± S.E.) correlation in the lap-by-lap Δrate (left) and ΔCOM (right) fluctuations for overlapping V1-CA1 cell pairs on different days. (D) Same as C, but for the correlation in modified Δrate and ΔCOM after removing the modulation by speed and head direction.DOI:http://dx.doi.org/10.7554/eLife.08902.015

Mentions: In our experiments, V1 and CA1 cells were recorded as the animals ran the same track for multiple days. We next analyzed how the activities of V1 location-responsive cells and CA1 place cells changed over the many days' experience of track running. We grouped the recording days to 3 different time points (T1–T3): T1 included Day 1 and 2, a novel condition to the animals, in which most of the behavioral changes occurred (Figure 1B,C), T3 included Day 6 to Day 7+, which we consider to be a familiar condition, and T2 included Days 3–5, an intermediate condition between novel and familiar. We examined 279 V1 and 628 CA1 cells at T1, 173 V1 and 519 CA1 cells at T2, and 212 V1 and 557 CA1 cells at T3 that were active on at least one trajectory. First, we found that there was a significant increase from T1 to T3 in the median overall firing rate of V1 cells (50% increase between T1 and T3; p < 0.0001, Kruskal–Wallis test including all data at T1, T2 and T3), but not in the median firing rate of CA1 cells (3% increase between T1 and T3; p = 0.079; Figure 7A). Second, there was a significant increase in the median SMI for both V1 (55% increase between T1 and T3; p < 0.0001) and CA1 cells (39% increase between T1 and T3; p < 0.0001; Figure 7B), suggesting an experience-dependent increase in the location-specificity of V1 cells at the time scale of days. Third, we examined the correlation in Δrate and ΔCOM between overlapping V1-CA1 cell pairs at different time points (N = 244 pairs at T1, 108 pairs at T2, 174 pairs at T3). For the Δrate correlation, there was no significant change from T1 to T3 (2% decrease between T1 and T3; p = 0.20, one-way ANOVA comparing all data at T1, T2 and T3; Figure 7C). This is also true for the modified Δrate correlation after the speed and head direction modulation was removed (19% increase between T1 and T3; p = 0.13; Figure 7D). For the ΔCOM correlation, there was a small, but statistically non-significant decrease from T1 to T3 (17% decrease between T1 and T3; p = 0.11, one-way ANOVA; Figure 7C). For the modified ΔCOM, the decrease was more prominent, but remained non-significant (33% decrease between T1 and T3; p = 0.088; Figure 7D). These data show that, although there was an indication of slightly decreased co-fluctuation between V1 and CA1 cells with experience, their functional interaction persisted as the animals became familiarized with the track. Taken together, day-to-day track experience was accompanied by an increase in the firing rate and location-specificity of V1 cells, which remained correlated in their lap-by-lap fluctuations with overlapping CA1 cells.10.7554/eLife.08902.015Figure 7.Experience dependence of V1 and CA1 firing activities on the C-shaped track.


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

Haggerty DC, Ji D - Elife (2015)

Experience dependence of V1 and CA1 firing activities on the C-shaped track.(A, B) Cumulative distributions of overall firing rate (A) and SMI (B) of active V1 and CA1 cells on different days (T1 – T3, see texts for definition). (C) The average (mean ± S.E.) correlation in the lap-by-lap Δrate (left) and ΔCOM (right) fluctuations for overlapping V1-CA1 cell pairs on different days. (D) Same as C, but for the correlation in modified Δrate and ΔCOM after removing the modulation by speed and head direction.DOI:http://dx.doi.org/10.7554/eLife.08902.015
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Related In: Results  -  Collection

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fig7: Experience dependence of V1 and CA1 firing activities on the C-shaped track.(A, B) Cumulative distributions of overall firing rate (A) and SMI (B) of active V1 and CA1 cells on different days (T1 – T3, see texts for definition). (C) The average (mean ± S.E.) correlation in the lap-by-lap Δrate (left) and ΔCOM (right) fluctuations for overlapping V1-CA1 cell pairs on different days. (D) Same as C, but for the correlation in modified Δrate and ΔCOM after removing the modulation by speed and head direction.DOI:http://dx.doi.org/10.7554/eLife.08902.015
Mentions: In our experiments, V1 and CA1 cells were recorded as the animals ran the same track for multiple days. We next analyzed how the activities of V1 location-responsive cells and CA1 place cells changed over the many days' experience of track running. We grouped the recording days to 3 different time points (T1–T3): T1 included Day 1 and 2, a novel condition to the animals, in which most of the behavioral changes occurred (Figure 1B,C), T3 included Day 6 to Day 7+, which we consider to be a familiar condition, and T2 included Days 3–5, an intermediate condition between novel and familiar. We examined 279 V1 and 628 CA1 cells at T1, 173 V1 and 519 CA1 cells at T2, and 212 V1 and 557 CA1 cells at T3 that were active on at least one trajectory. First, we found that there was a significant increase from T1 to T3 in the median overall firing rate of V1 cells (50% increase between T1 and T3; p < 0.0001, Kruskal–Wallis test including all data at T1, T2 and T3), but not in the median firing rate of CA1 cells (3% increase between T1 and T3; p = 0.079; Figure 7A). Second, there was a significant increase in the median SMI for both V1 (55% increase between T1 and T3; p < 0.0001) and CA1 cells (39% increase between T1 and T3; p < 0.0001; Figure 7B), suggesting an experience-dependent increase in the location-specificity of V1 cells at the time scale of days. Third, we examined the correlation in Δrate and ΔCOM between overlapping V1-CA1 cell pairs at different time points (N = 244 pairs at T1, 108 pairs at T2, 174 pairs at T3). For the Δrate correlation, there was no significant change from T1 to T3 (2% decrease between T1 and T3; p = 0.20, one-way ANOVA comparing all data at T1, T2 and T3; Figure 7C). This is also true for the modified Δrate correlation after the speed and head direction modulation was removed (19% increase between T1 and T3; p = 0.13; Figure 7D). For the ΔCOM correlation, there was a small, but statistically non-significant decrease from T1 to T3 (17% decrease between T1 and T3; p = 0.11, one-way ANOVA; Figure 7C). For the modified ΔCOM, the decrease was more prominent, but remained non-significant (33% decrease between T1 and T3; p = 0.088; Figure 7D). These data show that, although there was an indication of slightly decreased co-fluctuation between V1 and CA1 cells with experience, their functional interaction persisted as the animals became familiarized with the track. Taken together, day-to-day track experience was accompanied by an increase in the firing rate and location-specificity of V1 cells, which remained correlated in their lap-by-lap fluctuations with overlapping CA1 cells.10.7554/eLife.08902.015Figure 7.Experience dependence of V1 and CA1 firing activities on the C-shaped track.

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