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MEG can map short and long-term changes in brain activity following deep brain stimulation for chronic pain.

Mohseni HR, Smith PP, Parsons CE, Young KS, Hyam JA, Stein A, Stein JF, Green AL, Aziz TZ, Kringelbach ML - PLoS ONE (2012)

Bottom Line: We found significant changes in activity in pain-related regions including the pre-supplementary motor area, brainstem (periaqueductal gray) and dissociable parts of caudal and rostral ACC.We were also able to demonstrate long-term functional brain changes as a result of continuous DBS over one year, leading to specific changes in the activity in dissociable regions of caudal and rostral ACC.These results broaden our understanding of the underlying mechanisms of DBS in the human brain.

View Article: PubMed Central - PubMed

Affiliation: University Department of Psychiatry, University of Oxford, Oxford, United Kingdom.

ABSTRACT
Deep brain stimulation (DBS) has been shown to be clinically effective for some forms of treatment-resistant chronic pain, but the precise mechanisms of action are not well understood. Here, we present an analysis of magnetoencephalography (MEG) data from a patient with whole-body chronic pain, in order to investigate changes in neural activity induced by DBS for pain relief over both short- and long-term. This patient is one of the few cases treated using DBS of the anterior cingulate cortex (ACC). We demonstrate that a novel method, -beamforming, can be used to localise accurately brain activity despite the artefacts caused by the presence of DBS electrodes and stimulus pulses. The accuracy of our source localisation was verified by correlating the predicted DBS electrode positions with their actual positions. Using this beamforming method, we examined changes in whole-brain activity comparing pain relief achieved with deep brain stimulation (DBS ON) and compared with pain experienced with no stimulation (DBS OFF). We found significant changes in activity in pain-related regions including the pre-supplementary motor area, brainstem (periaqueductal gray) and dissociable parts of caudal and rostral ACC. In particular, when the patient reported experiencing pain, there was increased activity in different regions of ACC compared to when he experienced pain relief. We were also able to demonstrate long-term functional brain changes as a result of continuous DBS over one year, leading to specific changes in the activity in dissociable regions of caudal and rostral ACC. These results broaden our understanding of the underlying mechanisms of DBS in the human brain.

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Summary of changes in brain activity between DBS ON and OFF after one week and one year after surgery.Four main midline brain regions were identified that had increases in power following pain related changes when DBS was OFF: the pre-supplementary motor area (pre-SMA), caudal-ACC (c-ACC), rostral-ACC (r-ACC) and brainstem (periaqueductal grey, PAG). A) The figure shows the mid-sagittal slice with the contours of the reconstructed MEG sources at 10Hz using -beamformer with DBS OFF. Below each brain slice is shown the corresponding 3D mesh plot of the reconstructed neural activity in the mid-sagittal slice at 10Hz (with the lower electrode location inserted in red). B) Similarly, when DBS is ON, the figure shows the reconstructed MEG sources and the corresponding 3D mesh plot. This shows a decrease in activity in the caudal and rostral ACC with pain relief. C) One year later, after a continuous DBS, a similar pattern of changes in activity emerges when the patient is in pain (DBS OFF). D) Similarly, a decrease in activity in rostral ACC is evident following pain relief with DBS ON. Interestingly, the activity in the caudal ACC appears to be depressed during pain after one year of DBS and thus show a much smaller decrease in activity upon pain relief. This could be suggestive of plastic changes following long term DBS. Please note that the vertical axes (depicting normalised power) are the same for Figures A and B but not for Figures C and D. As can be seen from the figure, the power of the reconstructed sources is independent from the number of rejected channels (see Methods). It is also notable that the full width at half maximum (FWHM) of each peak is also independent from the number of rejected channels (e.g. see the pre-SMA). The number of rejected channels is therefore likely only to have a minor influence on the source space results.
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pone-0037993-g003: Summary of changes in brain activity between DBS ON and OFF after one week and one year after surgery.Four main midline brain regions were identified that had increases in power following pain related changes when DBS was OFF: the pre-supplementary motor area (pre-SMA), caudal-ACC (c-ACC), rostral-ACC (r-ACC) and brainstem (periaqueductal grey, PAG). A) The figure shows the mid-sagittal slice with the contours of the reconstructed MEG sources at 10Hz using -beamformer with DBS OFF. Below each brain slice is shown the corresponding 3D mesh plot of the reconstructed neural activity in the mid-sagittal slice at 10Hz (with the lower electrode location inserted in red). B) Similarly, when DBS is ON, the figure shows the reconstructed MEG sources and the corresponding 3D mesh plot. This shows a decrease in activity in the caudal and rostral ACC with pain relief. C) One year later, after a continuous DBS, a similar pattern of changes in activity emerges when the patient is in pain (DBS OFF). D) Similarly, a decrease in activity in rostral ACC is evident following pain relief with DBS ON. Interestingly, the activity in the caudal ACC appears to be depressed during pain after one year of DBS and thus show a much smaller decrease in activity upon pain relief. This could be suggestive of plastic changes following long term DBS. Please note that the vertical axes (depicting normalised power) are the same for Figures A and B but not for Figures C and D. As can be seen from the figure, the power of the reconstructed sources is independent from the number of rejected channels (see Methods). It is also notable that the full width at half maximum (FWHM) of each peak is also independent from the number of rejected channels (e.g. see the pre-SMA). The number of rejected channels is therefore likely only to have a minor influence on the source space results.

Mentions: We used MEG to investigate the changes in brain activity with DBS on and off, both short term (after one week) and long term (after one year). Figure 3 summarises the changes in brain activity after one week and one year in the mid-sagittal views. Figure 3A shows the reconstructed MEG sources at 10Hz using the -beamformer when the DBS stimulator was turned OFF one week after surgery. This figure shows increased activity in the pain-related areas: pre-supplementary motor area (pre-SMA), brainstem (PAG) and medial prefrontal areas (mainly ACC) compared with stimulation turned on (Figure 3B). During stimulation at this time, the patient reported almost complete pain relief; concurrently, activity in the r-ACC in particular, and also in the c-ACC is substantially lower than during stimulation.


MEG can map short and long-term changes in brain activity following deep brain stimulation for chronic pain.

Mohseni HR, Smith PP, Parsons CE, Young KS, Hyam JA, Stein A, Stein JF, Green AL, Aziz TZ, Kringelbach ML - PLoS ONE (2012)

Summary of changes in brain activity between DBS ON and OFF after one week and one year after surgery.Four main midline brain regions were identified that had increases in power following pain related changes when DBS was OFF: the pre-supplementary motor area (pre-SMA), caudal-ACC (c-ACC), rostral-ACC (r-ACC) and brainstem (periaqueductal grey, PAG). A) The figure shows the mid-sagittal slice with the contours of the reconstructed MEG sources at 10Hz using -beamformer with DBS OFF. Below each brain slice is shown the corresponding 3D mesh plot of the reconstructed neural activity in the mid-sagittal slice at 10Hz (with the lower electrode location inserted in red). B) Similarly, when DBS is ON, the figure shows the reconstructed MEG sources and the corresponding 3D mesh plot. This shows a decrease in activity in the caudal and rostral ACC with pain relief. C) One year later, after a continuous DBS, a similar pattern of changes in activity emerges when the patient is in pain (DBS OFF). D) Similarly, a decrease in activity in rostral ACC is evident following pain relief with DBS ON. Interestingly, the activity in the caudal ACC appears to be depressed during pain after one year of DBS and thus show a much smaller decrease in activity upon pain relief. This could be suggestive of plastic changes following long term DBS. Please note that the vertical axes (depicting normalised power) are the same for Figures A and B but not for Figures C and D. As can be seen from the figure, the power of the reconstructed sources is independent from the number of rejected channels (see Methods). It is also notable that the full width at half maximum (FWHM) of each peak is also independent from the number of rejected channels (e.g. see the pre-SMA). The number of rejected channels is therefore likely only to have a minor influence on the source space results.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3366994&req=5

pone-0037993-g003: Summary of changes in brain activity between DBS ON and OFF after one week and one year after surgery.Four main midline brain regions were identified that had increases in power following pain related changes when DBS was OFF: the pre-supplementary motor area (pre-SMA), caudal-ACC (c-ACC), rostral-ACC (r-ACC) and brainstem (periaqueductal grey, PAG). A) The figure shows the mid-sagittal slice with the contours of the reconstructed MEG sources at 10Hz using -beamformer with DBS OFF. Below each brain slice is shown the corresponding 3D mesh plot of the reconstructed neural activity in the mid-sagittal slice at 10Hz (with the lower electrode location inserted in red). B) Similarly, when DBS is ON, the figure shows the reconstructed MEG sources and the corresponding 3D mesh plot. This shows a decrease in activity in the caudal and rostral ACC with pain relief. C) One year later, after a continuous DBS, a similar pattern of changes in activity emerges when the patient is in pain (DBS OFF). D) Similarly, a decrease in activity in rostral ACC is evident following pain relief with DBS ON. Interestingly, the activity in the caudal ACC appears to be depressed during pain after one year of DBS and thus show a much smaller decrease in activity upon pain relief. This could be suggestive of plastic changes following long term DBS. Please note that the vertical axes (depicting normalised power) are the same for Figures A and B but not for Figures C and D. As can be seen from the figure, the power of the reconstructed sources is independent from the number of rejected channels (see Methods). It is also notable that the full width at half maximum (FWHM) of each peak is also independent from the number of rejected channels (e.g. see the pre-SMA). The number of rejected channels is therefore likely only to have a minor influence on the source space results.
Mentions: We used MEG to investigate the changes in brain activity with DBS on and off, both short term (after one week) and long term (after one year). Figure 3 summarises the changes in brain activity after one week and one year in the mid-sagittal views. Figure 3A shows the reconstructed MEG sources at 10Hz using the -beamformer when the DBS stimulator was turned OFF one week after surgery. This figure shows increased activity in the pain-related areas: pre-supplementary motor area (pre-SMA), brainstem (PAG) and medial prefrontal areas (mainly ACC) compared with stimulation turned on (Figure 3B). During stimulation at this time, the patient reported almost complete pain relief; concurrently, activity in the r-ACC in particular, and also in the c-ACC is substantially lower than during stimulation.

Bottom Line: We found significant changes in activity in pain-related regions including the pre-supplementary motor area, brainstem (periaqueductal gray) and dissociable parts of caudal and rostral ACC.We were also able to demonstrate long-term functional brain changes as a result of continuous DBS over one year, leading to specific changes in the activity in dissociable regions of caudal and rostral ACC.These results broaden our understanding of the underlying mechanisms of DBS in the human brain.

View Article: PubMed Central - PubMed

Affiliation: University Department of Psychiatry, University of Oxford, Oxford, United Kingdom.

ABSTRACT
Deep brain stimulation (DBS) has been shown to be clinically effective for some forms of treatment-resistant chronic pain, but the precise mechanisms of action are not well understood. Here, we present an analysis of magnetoencephalography (MEG) data from a patient with whole-body chronic pain, in order to investigate changes in neural activity induced by DBS for pain relief over both short- and long-term. This patient is one of the few cases treated using DBS of the anterior cingulate cortex (ACC). We demonstrate that a novel method, -beamforming, can be used to localise accurately brain activity despite the artefacts caused by the presence of DBS electrodes and stimulus pulses. The accuracy of our source localisation was verified by correlating the predicted DBS electrode positions with their actual positions. Using this beamforming method, we examined changes in whole-brain activity comparing pain relief achieved with deep brain stimulation (DBS ON) and compared with pain experienced with no stimulation (DBS OFF). We found significant changes in activity in pain-related regions including the pre-supplementary motor area, brainstem (periaqueductal gray) and dissociable parts of caudal and rostral ACC. In particular, when the patient reported experiencing pain, there was increased activity in different regions of ACC compared to when he experienced pain relief. We were also able to demonstrate long-term functional brain changes as a result of continuous DBS over one year, leading to specific changes in the activity in dissociable regions of caudal and rostral ACC. These results broaden our understanding of the underlying mechanisms of DBS in the human brain.

Show MeSH
Related in: MedlinePlus