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Coupled variability in primary sensory areas and the hippocampus during spontaneous activity

View Article: PubMed Central - PubMed

ABSTRACT

The cerebral cortex is an anatomically divided and functionally specialized structure. It includes distinct areas, which work on different states over time. The structural features of spiking activity in sensory cortices have been characterized during spontaneous and evoked activity. However, the coordination among cortical and sub-cortical neurons during spontaneous activity across different states remains poorly characterized. We addressed this issue by studying the temporal coupling of spiking variability recorded from primary sensory cortices and hippocampus of anesthetized or freely behaving rats. During spontaneous activity, spiking variability was highly correlated across primary cortical sensory areas at both small and large spatial scales, whereas the cortico-hippocampal correlation was modest. This general pattern of spiking variability was observed under urethane anesthesia, as well as during waking, slow-wave sleep and rapid-eye-movement sleep, and was unchanged by novel stimulation. These results support the notion that primary sensory areas are strongly coupled during spontaneous activity.

No MeSH data available.


Related in: MedlinePlus

Time-scale and influence of novelty in coupling variability across brain areas.(a) Group data (n = 8): coupling on global variability across different time scales. On the vertical axis is shown the correlation between the coefficient of variation of population rate found in primary sensory cortices: S1, V1, and HP, and on the horizontal axis is shown the different bin sizes for the calculated coefficients of variation, one per pair of area/animal. Highlighted is the default bin size used in the main text (50 ms). The median of rCV significantly differs from zero (p < 0.01) in all conditions. (b) Samples of spiking correlation matrices based on the activity found in HP, S1 and V1 during (left) pre-exposure, (middle) exposure, and (right) post-exposure to novel objects, sorted by loadings of first principal component calculated based on correlated spiking activity during exposure. (c) Group data (n = 8) of Pearson’s correlation among the coefficient of variation of neuronal population activity found in S1, V1 and HP during pre-exposure (pre), exposure (exp) and post-exposure (post) to novel objects. (d) General proposal for coupling in variability in cortical activity. At small spatial scales of local cortical neuronal populations in the primary sensory cortex and hippocampus, local neuronal populations (circles) show strong shared variability and share very similar levels of variability across time, whereas at large scales, the primary sensory areas do not necessarily share their level of variability (spiking mode) but strongly share timing when the variability changes This last type of shared variability is only modest between cortex and hippocampus. (e) Illustration of the variability axis.
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f3: Time-scale and influence of novelty in coupling variability across brain areas.(a) Group data (n = 8): coupling on global variability across different time scales. On the vertical axis is shown the correlation between the coefficient of variation of population rate found in primary sensory cortices: S1, V1, and HP, and on the horizontal axis is shown the different bin sizes for the calculated coefficients of variation, one per pair of area/animal. Highlighted is the default bin size used in the main text (50 ms). The median of rCV significantly differs from zero (p < 0.01) in all conditions. (b) Samples of spiking correlation matrices based on the activity found in HP, S1 and V1 during (left) pre-exposure, (middle) exposure, and (right) post-exposure to novel objects, sorted by loadings of first principal component calculated based on correlated spiking activity during exposure. (c) Group data (n = 8) of Pearson’s correlation among the coefficient of variation of neuronal population activity found in S1, V1 and HP during pre-exposure (pre), exposure (exp) and post-exposure (post) to novel objects. (d) General proposal for coupling in variability in cortical activity. At small spatial scales of local cortical neuronal populations in the primary sensory cortex and hippocampus, local neuronal populations (circles) show strong shared variability and share very similar levels of variability across time, whereas at large scales, the primary sensory areas do not necessarily share their level of variability (spiking mode) but strongly share timing when the variability changes This last type of shared variability is only modest between cortex and hippocampus. (e) Illustration of the variability axis.

Mentions: There is robust evidence regarding changes in cortical variability across different behavioral states10161833. However, the temporal coupling in variability, and in cortico-cortical and cortico-hippocampal activity, during different behavioral states remains unknown. Thus, segmentation of the data according to the three major behavioral states studied was also performed: waking (WK), slow wave sleep (SWS), and rapid eye movement sleep (REM)16. This analysis indicated that the cortical spiking activity during wakefulness had significantly higher variability coupling than that observed during both sleep states (Fig. 2d; p ≪ 0.01). In addition, cortico-hippocampal coupling (both S1-HP and V1-HP) was also smaller than that observed between cortical areas. Importantly, the group data analysis (total of single units isolated 685, #S1 = 209, #V1 = 227, and #HP = 249; see Table S1) showed that coupling among primary sensory areas (S1V1) was significant (Fig. 2e; Wilcoxon, pS1V1 = 0.012, pS1HP = 0.036 and pV1HP = 0.025), and higher (Fig. 2e; Kruskal-Wallis, p = 0.036) than the coupling between primary sensory areas and HP for longer periods of time (Table S1), across different time-scales (Kruskal-Wallis p < 0.01; Fig. 3a). There was also significant coupling among the brain areas studied (Fig. 2f) across behavioral states (Wilcoxon, p < 0.05), except for V1HP during SWS (p = 0.067). Analysis of the same brain area pair across behavioral states (#animals: nWK = 8, nSWS = 8, and nREM = 7), demonstrated a significant difference only in S1-HP between WK and SWS (p = 0.046) and a trend in S1-V1 between WK and SWS states (p = 0.115).


Coupled variability in primary sensory areas and the hippocampus during spontaneous activity
Time-scale and influence of novelty in coupling variability across brain areas.(a) Group data (n = 8): coupling on global variability across different time scales. On the vertical axis is shown the correlation between the coefficient of variation of population rate found in primary sensory cortices: S1, V1, and HP, and on the horizontal axis is shown the different bin sizes for the calculated coefficients of variation, one per pair of area/animal. Highlighted is the default bin size used in the main text (50 ms). The median of rCV significantly differs from zero (p < 0.01) in all conditions. (b) Samples of spiking correlation matrices based on the activity found in HP, S1 and V1 during (left) pre-exposure, (middle) exposure, and (right) post-exposure to novel objects, sorted by loadings of first principal component calculated based on correlated spiking activity during exposure. (c) Group data (n = 8) of Pearson’s correlation among the coefficient of variation of neuronal population activity found in S1, V1 and HP during pre-exposure (pre), exposure (exp) and post-exposure (post) to novel objects. (d) General proposal for coupling in variability in cortical activity. At small spatial scales of local cortical neuronal populations in the primary sensory cortex and hippocampus, local neuronal populations (circles) show strong shared variability and share very similar levels of variability across time, whereas at large scales, the primary sensory areas do not necessarily share their level of variability (spiking mode) but strongly share timing when the variability changes This last type of shared variability is only modest between cortex and hippocampus. (e) Illustration of the variability axis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5385523&req=5

f3: Time-scale and influence of novelty in coupling variability across brain areas.(a) Group data (n = 8): coupling on global variability across different time scales. On the vertical axis is shown the correlation between the coefficient of variation of population rate found in primary sensory cortices: S1, V1, and HP, and on the horizontal axis is shown the different bin sizes for the calculated coefficients of variation, one per pair of area/animal. Highlighted is the default bin size used in the main text (50 ms). The median of rCV significantly differs from zero (p < 0.01) in all conditions. (b) Samples of spiking correlation matrices based on the activity found in HP, S1 and V1 during (left) pre-exposure, (middle) exposure, and (right) post-exposure to novel objects, sorted by loadings of first principal component calculated based on correlated spiking activity during exposure. (c) Group data (n = 8) of Pearson’s correlation among the coefficient of variation of neuronal population activity found in S1, V1 and HP during pre-exposure (pre), exposure (exp) and post-exposure (post) to novel objects. (d) General proposal for coupling in variability in cortical activity. At small spatial scales of local cortical neuronal populations in the primary sensory cortex and hippocampus, local neuronal populations (circles) show strong shared variability and share very similar levels of variability across time, whereas at large scales, the primary sensory areas do not necessarily share their level of variability (spiking mode) but strongly share timing when the variability changes This last type of shared variability is only modest between cortex and hippocampus. (e) Illustration of the variability axis.
Mentions: There is robust evidence regarding changes in cortical variability across different behavioral states10161833. However, the temporal coupling in variability, and in cortico-cortical and cortico-hippocampal activity, during different behavioral states remains unknown. Thus, segmentation of the data according to the three major behavioral states studied was also performed: waking (WK), slow wave sleep (SWS), and rapid eye movement sleep (REM)16. This analysis indicated that the cortical spiking activity during wakefulness had significantly higher variability coupling than that observed during both sleep states (Fig. 2d; p ≪ 0.01). In addition, cortico-hippocampal coupling (both S1-HP and V1-HP) was also smaller than that observed between cortical areas. Importantly, the group data analysis (total of single units isolated 685, #S1 = 209, #V1 = 227, and #HP = 249; see Table S1) showed that coupling among primary sensory areas (S1V1) was significant (Fig. 2e; Wilcoxon, pS1V1 = 0.012, pS1HP = 0.036 and pV1HP = 0.025), and higher (Fig. 2e; Kruskal-Wallis, p = 0.036) than the coupling between primary sensory areas and HP for longer periods of time (Table S1), across different time-scales (Kruskal-Wallis p < 0.01; Fig. 3a). There was also significant coupling among the brain areas studied (Fig. 2f) across behavioral states (Wilcoxon, p < 0.05), except for V1HP during SWS (p = 0.067). Analysis of the same brain area pair across behavioral states (#animals: nWK = 8, nSWS = 8, and nREM = 7), demonstrated a significant difference only in S1-HP between WK and SWS (p = 0.046) and a trend in S1-V1 between WK and SWS states (p = 0.115).

View Article: PubMed Central - PubMed

ABSTRACT

The cerebral cortex is an anatomically divided and functionally specialized structure. It includes distinct areas, which work on different states over time. The structural features of spiking activity in sensory cortices have been characterized during spontaneous and evoked activity. However, the coordination among cortical and sub-cortical neurons during spontaneous activity across different states remains poorly characterized. We addressed this issue by studying the temporal coupling of spiking variability recorded from primary sensory cortices and hippocampus of anesthetized or freely behaving rats. During spontaneous activity, spiking variability was highly correlated across primary cortical sensory areas at both small and large spatial scales, whereas the cortico-hippocampal correlation was modest. This general pattern of spiking variability was observed under urethane anesthesia, as well as during waking, slow-wave sleep and rapid-eye-movement sleep, and was unchanged by novel stimulation. These results support the notion that primary sensory areas are strongly coupled during spontaneous activity.

No MeSH data available.


Related in: MedlinePlus