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Left frontal glioma induces functional connectivity changes in syntax-related networks.

Kinno R, Ohta S, Muragaki Y, Maruyama T, Sakai KL - Springerplus (2015)

Bottom Line: More specifically, these latter patients showed normal connectivity between the left fronto-parietal regions, as well as normal connectivity between the left triangular and orbital parts of the left inferior frontal gyrus.Our results indicate that these pathways are most crucial among the syntax-related networks.Both data from the activation patterns and functional connectivity, which are different in temporal domains, should thus be combined to assess any behavioral deficits associated with brain abnormalities.

View Article: PubMed Central - PubMed

Affiliation: Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902 Japan ; Division of Neurology, Department of Internal Medicine, Showa University Northern Yokohama Hospital, 35-1 Chigasaki-chuo, Tsuzuki-ku, Yokohama, Kanagawa, 224-8503 Japan ; CREST, Japan Science and Technology Agency, 7 Gobancho, Chiyoda-ku, Tokyo, 102-0076 Japan.

ABSTRACT

Background: A glioma leads to a global loss of functional connectivity among multiple regions. However, the relationships between performance/activation changes and functional connectivity remain unclear. Our previous studies (Brain 137:1193-1212; Brain Lang 110:71-80) have shown that a glioma in the left lateral premotor cortex or the opercular/triangular parts of the left inferior frontal gyrus causes agrammatic comprehension accompanied by abnormal activations in 14 syntax-related regions. We have also confirmed that a glioma in the other left frontal regions does not affect task performances and activation patterns.

Results: By a partial correlation method for the time-series functional magnetic resonance imaging data, we analyzed the functional connectivity in 21 patients with a left frontal glioma. We observed that almost all of the functional connectivity exhibited chaotic changes in the agrammatic patients. In contrast, some functional connectivity was preserved in an orderly manner in the patients who showed normal performances and activation patterns. More specifically, these latter patients showed normal connectivity between the left fronto-parietal regions, as well as normal connectivity between the left triangular and orbital parts of the left inferior frontal gyrus.

Conclusions: Our results indicate that these pathways are most crucial among the syntax-related networks. Both data from the activation patterns and functional connectivity, which are different in temporal domains, should thus be combined to assess any behavioral deficits associated with brain abnormalities.

No MeSH data available.


Related in: MedlinePlus

Orderly or chaotic functional connectivity within syntax-related networks. a Normal functional connectivity within syntax-related networks. A partial correlation matrix and mean Z values within/between the three networks are shown for the Normal group, together with a schematic of the three syntax-related networks (I, II, and III) in the right panel. In the partial correlation matrix, region pairs of “within networks” surrounded by red, green, and blue boxes correspond to Networks I, II, and III, respectively, whereas region pairs of “between networks” are surrounded by a black box for each network pair. All diagonal elements were shown in black. The r values reported in the previous study (Kinno et al. 2014) were here converted to Z values by using the Fisher r-to-Z transformation. Error bars in the bar graphs indicate the SEM for the multiple region pairs. In the schematic, the brain regions of Networks I, II, and III are shown in red,green, and blue, respectively. b–d A partial correlation matrix and mean Z values within/between the three networks in the LPMC (b), F3 (c), and Other (d) groups (novel results in the present study). Each of the three white asterisks in the matrix (d) indicates a higher level of functional connectivity significantly different from the abnormal connectivity (P < 0.05). These three connections are also denoted by curved lines and white asterisks in the schematic (a). In the matrix (d), a network pair of Networks III & I surrounded by a black box shows increased connectivity compared to the other network pairs. AG angular gyrus, F3O orbital part of the inferior frontal gyrus, F3op/F3t opercular/triangular parts of the inferior frontal gyrus, F3t triangular part of the inferior frontal gyrus, IPS intraparietal sulcus, L. left, LG lingual gyrus, LPMC lateral premotor cortex, n. nuclei, pMTG/ITG posterior middle/inferior temporal gyri, pre-SMA pre-supplementary motor area, pSTG/MTG posterior superior/middle temporal gyri, R. right.
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Fig1: Orderly or chaotic functional connectivity within syntax-related networks. a Normal functional connectivity within syntax-related networks. A partial correlation matrix and mean Z values within/between the three networks are shown for the Normal group, together with a schematic of the three syntax-related networks (I, II, and III) in the right panel. In the partial correlation matrix, region pairs of “within networks” surrounded by red, green, and blue boxes correspond to Networks I, II, and III, respectively, whereas region pairs of “between networks” are surrounded by a black box for each network pair. All diagonal elements were shown in black. The r values reported in the previous study (Kinno et al. 2014) were here converted to Z values by using the Fisher r-to-Z transformation. Error bars in the bar graphs indicate the SEM for the multiple region pairs. In the schematic, the brain regions of Networks I, II, and III are shown in red,green, and blue, respectively. b–d A partial correlation matrix and mean Z values within/between the three networks in the LPMC (b), F3 (c), and Other (d) groups (novel results in the present study). Each of the three white asterisks in the matrix (d) indicates a higher level of functional connectivity significantly different from the abnormal connectivity (P < 0.05). These three connections are also denoted by curved lines and white asterisks in the schematic (a). In the matrix (d), a network pair of Networks III & I surrounded by a black box shows increased connectivity compared to the other network pairs. AG angular gyrus, F3O orbital part of the inferior frontal gyrus, F3op/F3t opercular/triangular parts of the inferior frontal gyrus, F3t triangular part of the inferior frontal gyrus, IPS intraparietal sulcus, L. left, LG lingual gyrus, LPMC lateral premotor cortex, n. nuclei, pMTG/ITG posterior middle/inferior temporal gyri, pre-SMA pre-supplementary motor area, pSTG/MTG posterior superior/middle temporal gyri, R. right.

Mentions: The partial correlation matrix for the Normal group clearly demonstrated the existence of three separate syntax-related networks (Figure 1a). Indeed, all of the functional connectivity within those networks was positive (mean Z value, 0.18), while “cross-talk” between these networks was absent for the Normal group (mean Z value, 0.002). We defined a “network-boundary effect” as the significantly greater connectivity among the regions within individual networks compared with other connectivity. The mean Z values within individual networks were significantly greater than those between any two of the networks (one-tailed t test, P < 0.0001), confirming the network-boundary effects.Figure 1


Left frontal glioma induces functional connectivity changes in syntax-related networks.

Kinno R, Ohta S, Muragaki Y, Maruyama T, Sakai KL - Springerplus (2015)

Orderly or chaotic functional connectivity within syntax-related networks. a Normal functional connectivity within syntax-related networks. A partial correlation matrix and mean Z values within/between the three networks are shown for the Normal group, together with a schematic of the three syntax-related networks (I, II, and III) in the right panel. In the partial correlation matrix, region pairs of “within networks” surrounded by red, green, and blue boxes correspond to Networks I, II, and III, respectively, whereas region pairs of “between networks” are surrounded by a black box for each network pair. All diagonal elements were shown in black. The r values reported in the previous study (Kinno et al. 2014) were here converted to Z values by using the Fisher r-to-Z transformation. Error bars in the bar graphs indicate the SEM for the multiple region pairs. In the schematic, the brain regions of Networks I, II, and III are shown in red,green, and blue, respectively. b–d A partial correlation matrix and mean Z values within/between the three networks in the LPMC (b), F3 (c), and Other (d) groups (novel results in the present study). Each of the three white asterisks in the matrix (d) indicates a higher level of functional connectivity significantly different from the abnormal connectivity (P < 0.05). These three connections are also denoted by curved lines and white asterisks in the schematic (a). In the matrix (d), a network pair of Networks III & I surrounded by a black box shows increased connectivity compared to the other network pairs. AG angular gyrus, F3O orbital part of the inferior frontal gyrus, F3op/F3t opercular/triangular parts of the inferior frontal gyrus, F3t triangular part of the inferior frontal gyrus, IPS intraparietal sulcus, L. left, LG lingual gyrus, LPMC lateral premotor cortex, n. nuclei, pMTG/ITG posterior middle/inferior temporal gyri, pre-SMA pre-supplementary motor area, pSTG/MTG posterior superior/middle temporal gyri, R. right.
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Related In: Results  -  Collection

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Fig1: Orderly or chaotic functional connectivity within syntax-related networks. a Normal functional connectivity within syntax-related networks. A partial correlation matrix and mean Z values within/between the three networks are shown for the Normal group, together with a schematic of the three syntax-related networks (I, II, and III) in the right panel. In the partial correlation matrix, region pairs of “within networks” surrounded by red, green, and blue boxes correspond to Networks I, II, and III, respectively, whereas region pairs of “between networks” are surrounded by a black box for each network pair. All diagonal elements were shown in black. The r values reported in the previous study (Kinno et al. 2014) were here converted to Z values by using the Fisher r-to-Z transformation. Error bars in the bar graphs indicate the SEM for the multiple region pairs. In the schematic, the brain regions of Networks I, II, and III are shown in red,green, and blue, respectively. b–d A partial correlation matrix and mean Z values within/between the three networks in the LPMC (b), F3 (c), and Other (d) groups (novel results in the present study). Each of the three white asterisks in the matrix (d) indicates a higher level of functional connectivity significantly different from the abnormal connectivity (P < 0.05). These three connections are also denoted by curved lines and white asterisks in the schematic (a). In the matrix (d), a network pair of Networks III & I surrounded by a black box shows increased connectivity compared to the other network pairs. AG angular gyrus, F3O orbital part of the inferior frontal gyrus, F3op/F3t opercular/triangular parts of the inferior frontal gyrus, F3t triangular part of the inferior frontal gyrus, IPS intraparietal sulcus, L. left, LG lingual gyrus, LPMC lateral premotor cortex, n. nuclei, pMTG/ITG posterior middle/inferior temporal gyri, pre-SMA pre-supplementary motor area, pSTG/MTG posterior superior/middle temporal gyri, R. right.
Mentions: The partial correlation matrix for the Normal group clearly demonstrated the existence of three separate syntax-related networks (Figure 1a). Indeed, all of the functional connectivity within those networks was positive (mean Z value, 0.18), while “cross-talk” between these networks was absent for the Normal group (mean Z value, 0.002). We defined a “network-boundary effect” as the significantly greater connectivity among the regions within individual networks compared with other connectivity. The mean Z values within individual networks were significantly greater than those between any two of the networks (one-tailed t test, P < 0.0001), confirming the network-boundary effects.Figure 1

Bottom Line: More specifically, these latter patients showed normal connectivity between the left fronto-parietal regions, as well as normal connectivity between the left triangular and orbital parts of the left inferior frontal gyrus.Our results indicate that these pathways are most crucial among the syntax-related networks.Both data from the activation patterns and functional connectivity, which are different in temporal domains, should thus be combined to assess any behavioral deficits associated with brain abnormalities.

View Article: PubMed Central - PubMed

Affiliation: Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902 Japan ; Division of Neurology, Department of Internal Medicine, Showa University Northern Yokohama Hospital, 35-1 Chigasaki-chuo, Tsuzuki-ku, Yokohama, Kanagawa, 224-8503 Japan ; CREST, Japan Science and Technology Agency, 7 Gobancho, Chiyoda-ku, Tokyo, 102-0076 Japan.

ABSTRACT

Background: A glioma leads to a global loss of functional connectivity among multiple regions. However, the relationships between performance/activation changes and functional connectivity remain unclear. Our previous studies (Brain 137:1193-1212; Brain Lang 110:71-80) have shown that a glioma in the left lateral premotor cortex or the opercular/triangular parts of the left inferior frontal gyrus causes agrammatic comprehension accompanied by abnormal activations in 14 syntax-related regions. We have also confirmed that a glioma in the other left frontal regions does not affect task performances and activation patterns.

Results: By a partial correlation method for the time-series functional magnetic resonance imaging data, we analyzed the functional connectivity in 21 patients with a left frontal glioma. We observed that almost all of the functional connectivity exhibited chaotic changes in the agrammatic patients. In contrast, some functional connectivity was preserved in an orderly manner in the patients who showed normal performances and activation patterns. More specifically, these latter patients showed normal connectivity between the left fronto-parietal regions, as well as normal connectivity between the left triangular and orbital parts of the left inferior frontal gyrus.

Conclusions: Our results indicate that these pathways are most crucial among the syntax-related networks. Both data from the activation patterns and functional connectivity, which are different in temporal domains, should thus be combined to assess any behavioral deficits associated with brain abnormalities.

No MeSH data available.


Related in: MedlinePlus