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Cortical network architecture for context processing in primate brain.

Chao ZC, Nagasaka Y, Fujii N - Elife (2015)

Bottom Line: We extracted five context-related network structures including a bottom-up network during encoding and, seconds later, cue-dependent retrieval of the same network with the opposite top-down connectivity.These findings show that context is represented in the cortical network as distributed communication structures with dynamic information flows.This study provides a general methodology for recording and analyzing cortical network neuronal communication during cognition.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Adaptive Intelligence, RIKEN Brain Science Institute, Wako-shi, Japan.

ABSTRACT
Context is information linked to a situation that can guide behavior. In the brain, context is encoded by sensory processing and can later be retrieved from memory. How context is communicated within the cortical network in sensory and mnemonic forms is unknown due to the lack of methods for high-resolution, brain-wide neuronal recording and analysis. Here, we report the comprehensive architecture of a cortical network for context processing. Using hemisphere-wide, high-density electrocorticography, we measured large-scale neuronal activity from monkeys observing videos of agents interacting in situations with different contexts. We extracted five context-related network structures including a bottom-up network during encoding and, seconds later, cue-dependent retrieval of the same network with the opposite top-down connectivity. These findings show that context is represented in the cortical network as distributed communication structures with dynamic information flows. This study provides a general methodology for recording and analyzing cortical network neuronal communication during cognition.

No MeSH data available.


Related in: MedlinePlus

Coordination and co-activation of network structures.(A) Functional coordination: The coordination between structures was evaluated by the correlation coefficients between structures' context and response dependence (the differences shown in Figures 4A, 5A). Each panel illustrates how Structure i (y-axis) correlated with Structure j (x-axis) in context dependence in Rf (left), context dependence in Rn (middle), and response dependence (right). Significant correlations are indicated as asterisks (α = 0.05) (see ‘Materials and methods’). (B) Dynamic co-activation: The dynamics correlation was shown by correlation coefficients between structures' temporal and spectral activation. Each panel shows how Structure i correlated with Structure j in temporal dynamics (left) and frequency profile (right). Significant correlations are indicated as asterisks (α = 0.05). (C) Anatomical overlap: The anatomical similarity was indexed by the ratio of shared anatomical connections between structures. Each panel illustrates the ratio of the number of shared connections between Structures i and j and the total number of connections in Structure i. Results obtained from three subjects are shown separately. (D) Undirected pathways of connections shared by all structures for each subject (top), and those appearing in at least one structure for each subject (bottom). The lateral cortical surface is shown on the left for Subject 1, and on the right for Subjects 2 and 3. Shared pathways (lines) between two cortical areas (circles) of the top 1, 5, 10, and 25% connections are shown. Pathways with greater strengths are overlaid on those with weaker strengths.DOI:http://dx.doi.org/10.7554/eLife.06121.025
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fig6: Coordination and co-activation of network structures.(A) Functional coordination: The coordination between structures was evaluated by the correlation coefficients between structures' context and response dependence (the differences shown in Figures 4A, 5A). Each panel illustrates how Structure i (y-axis) correlated with Structure j (x-axis) in context dependence in Rf (left), context dependence in Rn (middle), and response dependence (right). Significant correlations are indicated as asterisks (α = 0.05) (see ‘Materials and methods’). (B) Dynamic co-activation: The dynamics correlation was shown by correlation coefficients between structures' temporal and spectral activation. Each panel shows how Structure i correlated with Structure j in temporal dynamics (left) and frequency profile (right). Significant correlations are indicated as asterisks (α = 0.05). (C) Anatomical overlap: The anatomical similarity was indexed by the ratio of shared anatomical connections between structures. Each panel illustrates the ratio of the number of shared connections between Structures i and j and the total number of connections in Structure i. Results obtained from three subjects are shown separately. (D) Undirected pathways of connections shared by all structures for each subject (top), and those appearing in at least one structure for each subject (bottom). The lateral cortical surface is shown on the left for Subject 1, and on the right for Subjects 2 and 3. Shared pathways (lines) between two cortical areas (circles) of the top 1, 5, 10, and 25% connections are shown. Pathways with greater strengths are overlaid on those with weaker strengths.DOI:http://dx.doi.org/10.7554/eLife.06121.025

Mentions: To study function, we evaluated how each structure's context and response dependence correlated with others', by measuring correlation coefficients of structures' differences in comparisons across contexts in Rf, across contexts in Rn, and across responses (Figure 6A) (detailed in the ‘Materials and methods’). Significant correlations between two structures indicated that one structure's activation affected another's, and vice versa, demonstrating a causal interdependence or a common external driver. Across contexts in Rf (Figure 6A, left), Structure 1 significantly correlated to Structures 3 and 4, which were themselves significantly correlated to Structure 5. However, across contexts in Rn (Figure 6A, middle), a significant correlation was found only between Structures 1 and 3. These results confirmed that sensory perception of the context stimuli could be significantly correlated to the formation of an abstract context, and, in turn this abstract context could be significantly correlated to its reactivation and top-down modulation when a response had high emotional valence. Across responses (Figure 6A, right), Structure 2 significantly correlated to Structure 4, which was itself significantly correlated to Structure 5. This indicated that that top-down modulation is the integration of response information and abstract context information.10.7554/eLife.06121.025Figure 6.Coordination and co-activation of network structures.


Cortical network architecture for context processing in primate brain.

Chao ZC, Nagasaka Y, Fujii N - Elife (2015)

Coordination and co-activation of network structures.(A) Functional coordination: The coordination between structures was evaluated by the correlation coefficients between structures' context and response dependence (the differences shown in Figures 4A, 5A). Each panel illustrates how Structure i (y-axis) correlated with Structure j (x-axis) in context dependence in Rf (left), context dependence in Rn (middle), and response dependence (right). Significant correlations are indicated as asterisks (α = 0.05) (see ‘Materials and methods’). (B) Dynamic co-activation: The dynamics correlation was shown by correlation coefficients between structures' temporal and spectral activation. Each panel shows how Structure i correlated with Structure j in temporal dynamics (left) and frequency profile (right). Significant correlations are indicated as asterisks (α = 0.05). (C) Anatomical overlap: The anatomical similarity was indexed by the ratio of shared anatomical connections between structures. Each panel illustrates the ratio of the number of shared connections between Structures i and j and the total number of connections in Structure i. Results obtained from three subjects are shown separately. (D) Undirected pathways of connections shared by all structures for each subject (top), and those appearing in at least one structure for each subject (bottom). The lateral cortical surface is shown on the left for Subject 1, and on the right for Subjects 2 and 3. Shared pathways (lines) between two cortical areas (circles) of the top 1, 5, 10, and 25% connections are shown. Pathways with greater strengths are overlaid on those with weaker strengths.DOI:http://dx.doi.org/10.7554/eLife.06121.025
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fig6: Coordination and co-activation of network structures.(A) Functional coordination: The coordination between structures was evaluated by the correlation coefficients between structures' context and response dependence (the differences shown in Figures 4A, 5A). Each panel illustrates how Structure i (y-axis) correlated with Structure j (x-axis) in context dependence in Rf (left), context dependence in Rn (middle), and response dependence (right). Significant correlations are indicated as asterisks (α = 0.05) (see ‘Materials and methods’). (B) Dynamic co-activation: The dynamics correlation was shown by correlation coefficients between structures' temporal and spectral activation. Each panel shows how Structure i correlated with Structure j in temporal dynamics (left) and frequency profile (right). Significant correlations are indicated as asterisks (α = 0.05). (C) Anatomical overlap: The anatomical similarity was indexed by the ratio of shared anatomical connections between structures. Each panel illustrates the ratio of the number of shared connections between Structures i and j and the total number of connections in Structure i. Results obtained from three subjects are shown separately. (D) Undirected pathways of connections shared by all structures for each subject (top), and those appearing in at least one structure for each subject (bottom). The lateral cortical surface is shown on the left for Subject 1, and on the right for Subjects 2 and 3. Shared pathways (lines) between two cortical areas (circles) of the top 1, 5, 10, and 25% connections are shown. Pathways with greater strengths are overlaid on those with weaker strengths.DOI:http://dx.doi.org/10.7554/eLife.06121.025
Mentions: To study function, we evaluated how each structure's context and response dependence correlated with others', by measuring correlation coefficients of structures' differences in comparisons across contexts in Rf, across contexts in Rn, and across responses (Figure 6A) (detailed in the ‘Materials and methods’). Significant correlations between two structures indicated that one structure's activation affected another's, and vice versa, demonstrating a causal interdependence or a common external driver. Across contexts in Rf (Figure 6A, left), Structure 1 significantly correlated to Structures 3 and 4, which were themselves significantly correlated to Structure 5. However, across contexts in Rn (Figure 6A, middle), a significant correlation was found only between Structures 1 and 3. These results confirmed that sensory perception of the context stimuli could be significantly correlated to the formation of an abstract context, and, in turn this abstract context could be significantly correlated to its reactivation and top-down modulation when a response had high emotional valence. Across responses (Figure 6A, right), Structure 2 significantly correlated to Structure 4, which was itself significantly correlated to Structure 5. This indicated that that top-down modulation is the integration of response information and abstract context information.10.7554/eLife.06121.025Figure 6.Coordination and co-activation of network structures.

Bottom Line: We extracted five context-related network structures including a bottom-up network during encoding and, seconds later, cue-dependent retrieval of the same network with the opposite top-down connectivity.These findings show that context is represented in the cortical network as distributed communication structures with dynamic information flows.This study provides a general methodology for recording and analyzing cortical network neuronal communication during cognition.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Adaptive Intelligence, RIKEN Brain Science Institute, Wako-shi, Japan.

ABSTRACT
Context is information linked to a situation that can guide behavior. In the brain, context is encoded by sensory processing and can later be retrieved from memory. How context is communicated within the cortical network in sensory and mnemonic forms is unknown due to the lack of methods for high-resolution, brain-wide neuronal recording and analysis. Here, we report the comprehensive architecture of a cortical network for context processing. Using hemisphere-wide, high-density electrocorticography, we measured large-scale neuronal activity from monkeys observing videos of agents interacting in situations with different contexts. We extracted five context-related network structures including a bottom-up network during encoding and, seconds later, cue-dependent retrieval of the same network with the opposite top-down connectivity. These findings show that context is represented in the cortical network as distributed communication structures with dynamic information flows. This study provides a general methodology for recording and analyzing cortical network neuronal communication during cognition.

No MeSH data available.


Related in: MedlinePlus