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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

V1 location-responsive cells showed much less lap-by-lap backward shift in their firing locations than CA1 place cells.(A) Average lap-by-lap changes in COM for V1 location-responsive cells (red, N = 670) and CA1 place cells (blue, N = 1743). The COM change of a firing field at each lap was computed relative to its stabilized value, which was the average of those values at laps #21–25. Solid lines: linear regressions between the COM change and lap numbers for the first 10 laps. It can be seen that the COMs of CA1 place fields significantly and systematically shifted backward (COM decreased with lap number) along the animal's moving direction (p < 0.0001, one-way ANOVA; Pearson's R = −0.89, p = 0.0006). The COMs of V1 firing fields appeared to shift backward during the first 5 laps or so, but fluctuated forward/backward in later laps. As a result, there was no significant change in COM (p = 0.09, one-way ANOVA) within the first 10 laps and no significant correlation between average COM change and lap number (Pearson's R = 0.10, p = 0.79). In addition, the average change in COM of V1 firing fields was significantly less than that of CA1 place fields within the first 10 laps (p < 0.0001, two-way ANOVA). (B) Same as A, but for lap-by-lap COM change of V1 and CA1 cells after removing the modulation by speed and head direction. The results are similar. There was a systematic backward shifting of the modified COM for CA1 place fields (p < 0.0001, one-way ANOVA; Pearson's R = 0.86, p = 0.0014), but not so for V1 firing fields (p = 0.13; R = 0.23, p = 0.53; comparison between CA1 and V1: p < 0.0001, two-way ANOVA). Therefore, the analysis indicates that V1 firing fields showed much less dynamics at the short-term lap-by-lap time scale than CA1 place fields.DOI:http://dx.doi.org/10.7554/eLife.08902.013
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fig6s5: V1 location-responsive cells showed much less lap-by-lap backward shift in their firing locations than CA1 place cells.(A) Average lap-by-lap changes in COM for V1 location-responsive cells (red, N = 670) and CA1 place cells (blue, N = 1743). The COM change of a firing field at each lap was computed relative to its stabilized value, which was the average of those values at laps #21–25. Solid lines: linear regressions between the COM change and lap numbers for the first 10 laps. It can be seen that the COMs of CA1 place fields significantly and systematically shifted backward (COM decreased with lap number) along the animal's moving direction (p < 0.0001, one-way ANOVA; Pearson's R = −0.89, p = 0.0006). The COMs of V1 firing fields appeared to shift backward during the first 5 laps or so, but fluctuated forward/backward in later laps. As a result, there was no significant change in COM (p = 0.09, one-way ANOVA) within the first 10 laps and no significant correlation between average COM change and lap number (Pearson's R = 0.10, p = 0.79). In addition, the average change in COM of V1 firing fields was significantly less than that of CA1 place fields within the first 10 laps (p < 0.0001, two-way ANOVA). (B) Same as A, but for lap-by-lap COM change of V1 and CA1 cells after removing the modulation by speed and head direction. The results are similar. There was a systematic backward shifting of the modified COM for CA1 place fields (p < 0.0001, one-way ANOVA; Pearson's R = 0.86, p = 0.0014), but not so for V1 firing fields (p = 0.13; R = 0.23, p = 0.53; comparison between CA1 and V1: p < 0.0001, two-way ANOVA). Therefore, the analysis indicates that V1 firing fields showed much less dynamics at the short-term lap-by-lap time scale than CA1 place fields.DOI:http://dx.doi.org/10.7554/eLife.08902.013

Mentions: The co-fluctuation of V1-CA1 cells suggests that those overlapping pairs of V1-CA1 cells with both displaying bidirectional firing should show the same type of directionality (prospective or retrospective firing), similarly as in previous reports on CA1 cells and entorhinal grid cells (De Almeida et al., 2012; Bieri et al., 2014). Our data yielded 4 such overlapping and 10 non-overlapping pairs of V1 and CA1 cells. We found that all the 4 overlapping pairs showed the same type of directionality, but only 5 of the 10 non-overlapping pairs did so whereas the other 5 showed the opposite directionality. Although the number of such bi-directional overlapping pairs is low (mainly due to the low percentage of bidirectional V1 and CA1 cells), the result is consistent with the correlated fluctuation in the firing rate and firing location between overlapping V1 and CA1 cells. In addition, CA1 cells are known to systematically shift their COMs backward lap by lap (Mehta et al., 1997, 2000), presumably as a result of synaptic plasticity (Ekstrom et al., 2001). To understand whether the observed co-fluctuation in COM between V1 and CA1 cells were related to this lap-by-lap plastic change, we examined the lap-by-lap shift in the COMs of V1 cells. Our analysis shows that, although there was a sign of backward shifting in V1 cells during the first 5 laps or so, the shift was not as robust as and much smaller than that of CA1 cells (Figure 6—figure supplement 5). The result suggests that V1 firing activities are less plastic than those of CA1 cells at this short time scale of laps (McClelland et al., 1995), and that the co-fluctuation between V1 and CA1 cells is not primarily driven by rapid plasticity in their firing activities.


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

Haggerty DC, Ji D - Elife (2015)

V1 location-responsive cells showed much less lap-by-lap backward shift in their firing locations than CA1 place cells.(A) Average lap-by-lap changes in COM for V1 location-responsive cells (red, N = 670) and CA1 place cells (blue, N = 1743). The COM change of a firing field at each lap was computed relative to its stabilized value, which was the average of those values at laps #21–25. Solid lines: linear regressions between the COM change and lap numbers for the first 10 laps. It can be seen that the COMs of CA1 place fields significantly and systematically shifted backward (COM decreased with lap number) along the animal's moving direction (p < 0.0001, one-way ANOVA; Pearson's R = −0.89, p = 0.0006). The COMs of V1 firing fields appeared to shift backward during the first 5 laps or so, but fluctuated forward/backward in later laps. As a result, there was no significant change in COM (p = 0.09, one-way ANOVA) within the first 10 laps and no significant correlation between average COM change and lap number (Pearson's R = 0.10, p = 0.79). In addition, the average change in COM of V1 firing fields was significantly less than that of CA1 place fields within the first 10 laps (p < 0.0001, two-way ANOVA). (B) Same as A, but for lap-by-lap COM change of V1 and CA1 cells after removing the modulation by speed and head direction. The results are similar. There was a systematic backward shifting of the modified COM for CA1 place fields (p < 0.0001, one-way ANOVA; Pearson's R = 0.86, p = 0.0014), but not so for V1 firing fields (p = 0.13; R = 0.23, p = 0.53; comparison between CA1 and V1: p < 0.0001, two-way ANOVA). Therefore, the analysis indicates that V1 firing fields showed much less dynamics at the short-term lap-by-lap time scale than CA1 place fields.DOI:http://dx.doi.org/10.7554/eLife.08902.013
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fig6s5: V1 location-responsive cells showed much less lap-by-lap backward shift in their firing locations than CA1 place cells.(A) Average lap-by-lap changes in COM for V1 location-responsive cells (red, N = 670) and CA1 place cells (blue, N = 1743). The COM change of a firing field at each lap was computed relative to its stabilized value, which was the average of those values at laps #21–25. Solid lines: linear regressions between the COM change and lap numbers for the first 10 laps. It can be seen that the COMs of CA1 place fields significantly and systematically shifted backward (COM decreased with lap number) along the animal's moving direction (p < 0.0001, one-way ANOVA; Pearson's R = −0.89, p = 0.0006). The COMs of V1 firing fields appeared to shift backward during the first 5 laps or so, but fluctuated forward/backward in later laps. As a result, there was no significant change in COM (p = 0.09, one-way ANOVA) within the first 10 laps and no significant correlation between average COM change and lap number (Pearson's R = 0.10, p = 0.79). In addition, the average change in COM of V1 firing fields was significantly less than that of CA1 place fields within the first 10 laps (p < 0.0001, two-way ANOVA). (B) Same as A, but for lap-by-lap COM change of V1 and CA1 cells after removing the modulation by speed and head direction. The results are similar. There was a systematic backward shifting of the modified COM for CA1 place fields (p < 0.0001, one-way ANOVA; Pearson's R = 0.86, p = 0.0014), but not so for V1 firing fields (p = 0.13; R = 0.23, p = 0.53; comparison between CA1 and V1: p < 0.0001, two-way ANOVA). Therefore, the analysis indicates that V1 firing fields showed much less dynamics at the short-term lap-by-lap time scale than CA1 place fields.DOI:http://dx.doi.org/10.7554/eLife.08902.013
Mentions: The co-fluctuation of V1-CA1 cells suggests that those overlapping pairs of V1-CA1 cells with both displaying bidirectional firing should show the same type of directionality (prospective or retrospective firing), similarly as in previous reports on CA1 cells and entorhinal grid cells (De Almeida et al., 2012; Bieri et al., 2014). Our data yielded 4 such overlapping and 10 non-overlapping pairs of V1 and CA1 cells. We found that all the 4 overlapping pairs showed the same type of directionality, but only 5 of the 10 non-overlapping pairs did so whereas the other 5 showed the opposite directionality. Although the number of such bi-directional overlapping pairs is low (mainly due to the low percentage of bidirectional V1 and CA1 cells), the result is consistent with the correlated fluctuation in the firing rate and firing location between overlapping V1 and CA1 cells. In addition, CA1 cells are known to systematically shift their COMs backward lap by lap (Mehta et al., 1997, 2000), presumably as a result of synaptic plasticity (Ekstrom et al., 2001). To understand whether the observed co-fluctuation in COM between V1 and CA1 cells were related to this lap-by-lap plastic change, we examined the lap-by-lap shift in the COMs of V1 cells. Our analysis shows that, although there was a sign of backward shifting in V1 cells during the first 5 laps or so, the shift was not as robust as and much smaller than that of CA1 cells (Figure 6—figure supplement 5). The result suggests that V1 firing activities are less plastic than those of CA1 cells at this short time scale of laps (McClelland et al., 1995), and that the co-fluctuation between V1 and CA1 cells is not primarily driven by rapid plasticity in their firing activities.

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