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Complexity measures in magnetoencephalography: measuring "disorder" in schizophrenia.

Brookes MJ, Hall EL, Robson SE, Price D, Palaniyappan L, Liddle EB, Liddle PF, Robinson SE, Morris PG - PLoS ONE (2015)

Bottom Line: These time-courses are modulated by cognitive tasks, with an increase in local neural processing characterised by localised and transient increases in entropy in the neural signal.We observe a direct but complex relationship between entropy and oscillatory amplitude, which suggests that these metrics are complementary.We demonstrate significantly increased task induced entropy change in patients (compared to controls) in multiple brain regions, including a cingulo-insula network, bilateral insula cortices and a right fronto-parietal network.

View Article: PubMed Central - PubMed

Affiliation: Sir Peter Mansfield Magnetic Resonance Centre, School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.

ABSTRACT
This paper details a methodology which, when applied to magnetoencephalography (MEG) data, is capable of measuring the spatio-temporal dynamics of 'disorder' in the human brain. Our method, which is based upon signal entropy, shows that spatially separate brain regions (or networks) generate temporally independent entropy time-courses. These time-courses are modulated by cognitive tasks, with an increase in local neural processing characterised by localised and transient increases in entropy in the neural signal. We explore the relationship between entropy and the more established time-frequency decomposition methods, which elucidate the temporal evolution of neural oscillations. We observe a direct but complex relationship between entropy and oscillatory amplitude, which suggests that these metrics are complementary. Finally, we provide a demonstration of the clinical utility of our method, using it to shed light on aberrant neurophysiological processing in schizophrenia. We demonstrate significantly increased task induced entropy change in patients (compared to controls) in multiple brain regions, including a cingulo-insula network, bilateral insula cortices and a right fronto-parietal network. These findings demonstrate potential clinical utility for our method and support a recent hypothesis that schizophrenia can be characterised by abnormalities in the salience network (a well characterised distributed network comprising bilateral insula and cingulate cortices).

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Related in: MedlinePlus

Time-courses in the visual cortex (A), cingulo-insula cortex (B), left motor cortex (C) and right motor cortex (D) showing task induced change in baseline entropy.Results are presented for schizophrenia patients (red) and healthy control subjects (blue) in the relevant and irrelevant phase of the RM task, and the Sternberg task. Bar charts show averaged entropy change during task, compared to rest, collapsed across both tasks. Note that in the cingulo-insula cortex, a significant (corrected p < 0.05) increase in entropy in patients, relative to control subjects is observed. Note also that the difference between patients and controls changes as a function of time, highlighting the importance of dynamic assessment of entropy.
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pone.0120991.g007: Time-courses in the visual cortex (A), cingulo-insula cortex (B), left motor cortex (C) and right motor cortex (D) showing task induced change in baseline entropy.Results are presented for schizophrenia patients (red) and healthy control subjects (blue) in the relevant and irrelevant phase of the RM task, and the Sternberg task. Bar charts show averaged entropy change during task, compared to rest, collapsed across both tasks. Note that in the cingulo-insula cortex, a significant (corrected p < 0.05) increase in entropy in patients, relative to control subjects is observed. Note also that the difference between patients and controls changes as a function of time, highlighting the importance of dynamic assessment of entropy.

Mentions: Fig 7 shows trial averaged entropy time-courses, for the Sternberg and RM tasks, for control subjects (blue) and schizophrenia patients (red). Results are shown for the visual cortex (A), the cingulo-insula component (B), the left motor cortex (C) and the right motor cortex (D). As with the entropy metrics in Fig 5, the zero-line represents resting entropy, and time-courses show stimulus induced change from baseline. The bar charts in Fig 7 show mean task induced entropy change in healthy controls (left) and patients (right) for each region; these measurements are collapsed across subjects and tasks (i.e. 22 independent MEG sessions in each group) and error bars show standard error across subjects. The principal result, summarised by Fig 7B, shows that in the cingulo-insula cortex, task induced entropy change is higher in patients than controls. The between group difference was found to be significant at a p<0.05 level, Bonferroni corrected across the 12 brain regions studied (this was true both using permutation testing, and a non-parametric Wilcoxon sum-rank test). In addition to the cingulo-insula component, significantly increased entropy was recorded in both the left and right insula cortices and the right fronto-parietal network. None of the other brain regions in Fig 4 reached statistical significance although a trend was noted in the left motor cortex.


Complexity measures in magnetoencephalography: measuring "disorder" in schizophrenia.

Brookes MJ, Hall EL, Robson SE, Price D, Palaniyappan L, Liddle EB, Liddle PF, Robinson SE, Morris PG - PLoS ONE (2015)

Time-courses in the visual cortex (A), cingulo-insula cortex (B), left motor cortex (C) and right motor cortex (D) showing task induced change in baseline entropy.Results are presented for schizophrenia patients (red) and healthy control subjects (blue) in the relevant and irrelevant phase of the RM task, and the Sternberg task. Bar charts show averaged entropy change during task, compared to rest, collapsed across both tasks. Note that in the cingulo-insula cortex, a significant (corrected p < 0.05) increase in entropy in patients, relative to control subjects is observed. Note also that the difference between patients and controls changes as a function of time, highlighting the importance of dynamic assessment of entropy.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401778&req=5

pone.0120991.g007: Time-courses in the visual cortex (A), cingulo-insula cortex (B), left motor cortex (C) and right motor cortex (D) showing task induced change in baseline entropy.Results are presented for schizophrenia patients (red) and healthy control subjects (blue) in the relevant and irrelevant phase of the RM task, and the Sternberg task. Bar charts show averaged entropy change during task, compared to rest, collapsed across both tasks. Note that in the cingulo-insula cortex, a significant (corrected p < 0.05) increase in entropy in patients, relative to control subjects is observed. Note also that the difference between patients and controls changes as a function of time, highlighting the importance of dynamic assessment of entropy.
Mentions: Fig 7 shows trial averaged entropy time-courses, for the Sternberg and RM tasks, for control subjects (blue) and schizophrenia patients (red). Results are shown for the visual cortex (A), the cingulo-insula component (B), the left motor cortex (C) and the right motor cortex (D). As with the entropy metrics in Fig 5, the zero-line represents resting entropy, and time-courses show stimulus induced change from baseline. The bar charts in Fig 7 show mean task induced entropy change in healthy controls (left) and patients (right) for each region; these measurements are collapsed across subjects and tasks (i.e. 22 independent MEG sessions in each group) and error bars show standard error across subjects. The principal result, summarised by Fig 7B, shows that in the cingulo-insula cortex, task induced entropy change is higher in patients than controls. The between group difference was found to be significant at a p<0.05 level, Bonferroni corrected across the 12 brain regions studied (this was true both using permutation testing, and a non-parametric Wilcoxon sum-rank test). In addition to the cingulo-insula component, significantly increased entropy was recorded in both the left and right insula cortices and the right fronto-parietal network. None of the other brain regions in Fig 4 reached statistical significance although a trend was noted in the left motor cortex.

Bottom Line: These time-courses are modulated by cognitive tasks, with an increase in local neural processing characterised by localised and transient increases in entropy in the neural signal.We observe a direct but complex relationship between entropy and oscillatory amplitude, which suggests that these metrics are complementary.We demonstrate significantly increased task induced entropy change in patients (compared to controls) in multiple brain regions, including a cingulo-insula network, bilateral insula cortices and a right fronto-parietal network.

View Article: PubMed Central - PubMed

Affiliation: Sir Peter Mansfield Magnetic Resonance Centre, School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.

ABSTRACT
This paper details a methodology which, when applied to magnetoencephalography (MEG) data, is capable of measuring the spatio-temporal dynamics of 'disorder' in the human brain. Our method, which is based upon signal entropy, shows that spatially separate brain regions (or networks) generate temporally independent entropy time-courses. These time-courses are modulated by cognitive tasks, with an increase in local neural processing characterised by localised and transient increases in entropy in the neural signal. We explore the relationship between entropy and the more established time-frequency decomposition methods, which elucidate the temporal evolution of neural oscillations. We observe a direct but complex relationship between entropy and oscillatory amplitude, which suggests that these metrics are complementary. Finally, we provide a demonstration of the clinical utility of our method, using it to shed light on aberrant neurophysiological processing in schizophrenia. We demonstrate significantly increased task induced entropy change in patients (compared to controls) in multiple brain regions, including a cingulo-insula network, bilateral insula cortices and a right fronto-parietal network. These findings demonstrate potential clinical utility for our method and support a recent hypothesis that schizophrenia can be characterised by abnormalities in the salience network (a well characterised distributed network comprising bilateral insula and cingulate cortices).

Show MeSH
Related in: MedlinePlus