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Effective connectivity analysis of inter- and intramodular hubs in phantom sound perception – identifying the core distress network

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Abstract

Tinnitus, the perception of a phantom sound, is accompanied by loudness and distress components. Distress however accompanies not just tinnitus, but several disorders. Several functional connectivity studies show that distress is characterized by disconnectivity of fronto-limbic circuits or hyperconnectivity of default mode/salience networks. The drawback, however, is that it considers only the magnitude of connectivity, not the direction. Thus, the current study aims to identify the core network of the domain-general distress component in tinnitus by comparing whole brain directed functional networks calculated from 5 min of resting state EEG data collected from 310 tinnitus patients and 256 non-tinnitus controls. We observe a reorganization of the overall tinnitus network, reflected by a decrease in strength and efficiency of information transfer between fronto-limbic and medial temporal regions, forming the main hubs of the tinnitus network. Further, a disconnection amongst a subset of these connections was observed to correlate with distress, forming a core distress network. The core distress network showed a decrease in strength of connections specifically going from the left hippocampus/parahippocampus to the subgenual anterior cingulate cortex. Such a disconnection suggests that the parahippocampal contextual memory has little influence on the (paradoxical) value that is attached to the phantom sound and that distress is the consequence of the absence of modulation of the phantom sound.

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Correspondence to Sven Vanneste.

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The authors declare no competing financial or conflict of other interests.

Research involving human participants

This study was approved by the local ethical committee (Antwerp University Hospital) and was in accordance with the declaration of Helsinki. Collection of the data was done under the approval of IRB UZA OGA85. All patients gave their written informed consent.

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Supplementary Fig 1

Schematic of the 84 Brodmann areas used in the study. Each black circle is a node which represents each Brodmann area. (PNG 16665 kb) (PNG 9217 kb)

High Resolution Image (TIF 2760 kb)

Supplementary Fig 2

Comparison of path length between the controls and tinnitus at the connection level. (a, b) depict the path length of the effective connectivity network in the control and tinnitus group respectively and the significant difference in path length before (c) and after (d) Bonferroni correction in the alpha1 frequency band. Similarly, (e, f) depict the path length of the effective connectivity network in the control and tinnitus group respectively and the significant difference in path length before (g) and after (h) Bonferroni correction in the alpha2 frequency band. Connections with significantly greater path length in controls are shown in black, connections with significantly greater path length in tinnitus are shown in red and connections with no significant difference in path length are shown in white. (PNG 16665 kb)

High Resolution Image (TIF 5123 kb)

Supplementary Fig 3

Community structure of the average control (left panel) and tinnitus (right panel) networks in the two alpha frequency bands (a–b) alpha1, (c - d) alpha2. (PNG 18087 kb)

High Resolution Image (TIF 4346 kb)

Supplementary Fig 4

Classification of peripheral nodes, connector nodes, provincial hubs and connector hubs in the average control (left panel) and tinnitus (right panel) network in the two alpha frequency bands (a - b) alpha1, (c - d) alpha2. (PNG 4573 kb)

High Resolution Image (TIF 1359 kb)

Supplementary Fig 5

Comparison of path length between the distinct hubs of tinnitus network with corresponding connections in the control network. (a-d) depict the path length between specific regions in the (a) control group; (b) tinnitus group; (c, d) the significant difference in path length between controls and tinnitus before and after Bonferroni correction respectively in the alpha1 frequency band. Similarly, (e-h) depict the path length between specific nodes in the (e) control group; (f) tinnitus group; (g, h) the significant difference in path length between controls and tinnitus before and after Bonferroni correction respectively in the alpha2 frequency band. Connections with significantly greater path length in controls are shown in black, connections with significantly greater path length in tinnitus are shown in red and connections with no significant difference in path length are shown in white. (PNG 4619 kb)

High Resolution Image (TIF 2117 kb)

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Mohan, A., Davidson, C., De Ridder, D. et al. Effective connectivity analysis of inter- and intramodular hubs in phantom sound perception – identifying the core distress network. Brain Imaging and Behavior 14, 289–307 (2020). https://doi.org/10.1007/s11682-018-9989-7

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  • DOI: https://doi.org/10.1007/s11682-018-9989-7

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