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Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex.

ABSTRACT: Everyday circumstances require efficient updating of behavior. Brain systems in the right inferior frontal cortex have been identified as critical for some aspects of behavioral updating, such as stopping actions. However, the precise role of these neural systems is controversial. Here we examined how the inferior frontal cortex updates behavior by combining reversible cortical interference (transcranial magnetic stimulation) with an experimental task that measures different types of updating. We found that the right inferior frontal cortex can be functionally segregated into two subregions: a dorsal region, which is critical for visual detection of changes in the environment, and a ventral region, which updates the corresponding action plan. This dissociation reconciles competing accounts of prefrontal organization and casts light on the neural architecture of human cognitive control.

SUBMITTER: Verbruggen F

PROVIDER: S-EPMC2922216 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex.

Verbruggen Frederick F Aron Adam R AR Stevens Michaël A MA Chambers Christopher D CD

Proceedings of the National Academy of Sciences of the United States of America 20100714 31

Everyday circumstances require efficient updating of behavior. Brain systems in the right inferior frontal cortex have been identified as critical for some aspects of behavioral updating, such as stopping actions. However, the precise role of these neural systems is controversial. Here we examined how the inferior frontal cortex updates behavior by combining reversible cortical interference (transcranial magnetic stimulation) with an experimental task that measures different types of updating. W ...[more]

PMID: 20631303

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Project description:Non-invasive brain stimulation is a useful tool to probe brain function and provide therapeutic treatments in disease. When applied to the right posterior parietal cortex (PPC) of healthy participants, it is possible to temporarily shift spatial attention and mimic symptoms of spatial neglect. However, the field of brain stimulation is plagued by issues of high response variability. The aim of this study was to investigate baseline functional connectivity as a predictor of response to an inhibitory brain stimulation paradigm applied to the right PPC. In fourteen healthy adults (9 female, aged 24.8 ± 4.0 years) we applied continuous theta burst stimulation (cTBS) to suppress activity in the right PPC. Resting state functional connectivity was quantified by recording electroencephalography and assessing phase consistency. Spatial attention was assessed before and after cTBS with the Landmark Task. Finally, known determinants of response to brain stimulation were controlled for to enable robust investigation of the influence of resting state connectivity on cTBS response. We observed significant inter-individual variability in the behavioral response to cTBS with 53.8% of participants demonstrating the expected rightward shift in spatial attention. Baseline high beta connectivity between the right PPC, dorsomedial pre-motor region and left temporal-parietal region was strongly associated with cTBS response (R 2 = 0.51). Regression analysis combining known cTBS determinants (age, sex, motor threshold, physical activity, stress) found connectivity between the right PPC and left temporal-parietal region was the only significant variable (p = 0.011). These results suggest baseline resting state functional connectivity is a strong predictor of a shift in spatial attention following cTBS. Findings from this study help further understand the mechanism by which cTBS modifies cortical function and could be used to improve the reliability of brain stimulation protocols.

Project description:Introduction:Cognitive symptoms from Parkinson's disease cause severe disability and significantly limit quality of life. Little is known about mechanisms of cognitive impairment in PD, although aberrant oscillatory activity in basal ganglia-thalamo-prefrontal cortical circuits likely plays an important role. While continuous high-frequency deep brain stimulation (DBS) improves motor symptoms, it is generally ineffective for cognitive symptoms. Although we lack robust treatment options for these symptoms, recent studies with transcranial magnetic stimulation (TMS), applying intermittent theta-burst stimulation (iTBS) to dorsolateral prefrontal cortex (DLPFC), suggest beneficial effects for certain aspects of cognition, such as memory or inhibitory control. While TMS is non-invasive, its results are transient and require repeated application. Subcortical DBS targets have strong reciprocal connections with prefrontal cortex, such that iTBS through the permanently implanted lead might represent a more durable solution. Here we demonstrate safety and feasibility for delivering iTBS from the DBS electrode and explore changes in DLPFC electrophysiology. Methods:We enrolled seven participants with medically refractory Parkinson's disease who underwent DBS surgery targeting either the subthalamic nucleus (STN) or globus pallidus interna (GPi). We temporarily placed an electrocorticography strip over DLPFC through the DBS burr hole. After placement of the DBS electrode into either GPi (n = 3) or STN (n = 4), awake subjects rested quietly during iTBS (three 50-Hz pulses delivered at 5 Hz for 2 s, followed by 8 s of rest). We contrasted power spectra in DLPFC local field potentials during iTBS versus at rest, as well as between iTBS and conventional high-frequency stimulation (HFS). Results:Dominant frequencies in DLPFC at rest varied among subjects and along the subdural strip electrode, though they were generally localized in theta (3-8 Hz) and/or beta (10-30 Hz) ranges. Both iTBS and HFS were well-tolerated and imperceptible. iTBS increased theta-frequency activity more than HFS. Further, GPi stimulation resulted in significantly greater theta-power versus STN stimulation in our sample. Conclusion:Acute subcortical iTBS from the DBS electrode was safe and well-tolerated. This novel stimulation pattern delivered from the GPi may increase theta-frequency power in ipsilateral DLPFC. Future studies will confirm these changes in DLPFC activity during iTBS and evaluate whether they are associated with improvements in cognitive or behavioral symptoms from PD.

Dataset Information

Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex.

Publications

Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex.

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