scholarly journals Amplified engagement of prefrontal cortex during control of voluntary action in Tourette syndrome

2020 ◽  
Vol 2 (2) ◽  
Author(s):  
Charlotte L Rae ◽  
Jim Parkinson ◽  
Sophie Betka ◽  
Cassandra D Gouldvan Praag ◽  
Samira Bouyagoub ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Motor Cortex ◽  
Caudate Nucleus ◽  
Tourette Syndrome ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Inferior Frontal Gyrus ◽  
Voluntary Action ◽  
Reactive Inhibition ◽  
Tic Suppression

Abstract Tourette syndrome is characterized by ‘unvoluntary’ tics, which are compulsive, yet often temporarily suppressible. The inferior frontal gyrus is implicated in motor control, including inhibition of pre-potent actions through influences on downstream subcortical and motor regions. Although tic suppression in Tourette syndrome also engages the inferior frontal gyrus, it is unclear whether such prefrontal control of action is also dysfunctional: Tic suppression studies do not permit comparison with control groups, and neuroimaging studies of motor inhibition can be confounded by the concurrent expression or suppression of tics. Here, patients with Tourette syndrome were directly compared to control participants when performing an intentional inhibition task during functional MRI. Tic expression was recorded throughout for removal from statistical models. Participants were instructed to make a button press in response to Go cues, withhold responses to NoGo cues, and decide whether to press or withhold to ‘Choose’ cues. Overall performance was similar between groups, for both intentional inhibition rates (% Choose-Go) and reactive NoGo inhibition commission errors. A subliminal face prime elicited no additional effects on intentional or reactive inhibition. Across participants, the task activated prefrontal and motor cortices and subcortical nuclei, including pre-supplementary motor area, inferior frontal gyrus, insula, caudate nucleus, thalamus and primary motor cortex. In Tourette syndrome, activity was elevated in the inferior frontal gyrus, insula and basal ganglia, most notably within the right inferior frontal gyrus during voluntary action and inhibition (Choose-Go and Choose-NoGo), and reactive inhibition (NoGo-correct). Anatomically, the locus of this inferior frontal gyrus hyperactivation during control of voluntary action matched that previously reported for tic suppression. In Tourette syndrome, activity within the caudate nucleus was also enhanced during both intentional (Choose-NoGo) and reactive (NoGo-correct) inhibition. Strikingly, despite the absence of overt motor behaviour, primary motor cortex activity increased in patients with Tourette syndrome but decreased in controls during both reactive and intentional inhibition. Additionally, severity of premonitory sensations scaled with functional connectivity of the pre-supplementary motor area to the caudate nucleus, globus pallidus and thalamus when choosing to respond (Choose-Go). Together, these results suggest that patients with Tourette syndrome use equivalent prefrontal mechanisms to suppress tics and withhold non-tic actions, but require greater inferior frontal gyrus engagement than controls to overcome motor drive from hyperactive downstream regions, notably primary motor cortex. Moreover, premonitory sensations may cue midline motor regions to generate tics through interactions with the basal ganglia.

scholarly journals Amplified engagement of prefrontal cortex during control of voluntary action in Tourette syndrome

2020 ◽  
Author(s):  
Charlotte Rae
Keyword(s):  
Basal Ganglia ◽  
Motor Cortex ◽  
Caudate Nucleus ◽  
Tourette Syndrome ◽  
Primary Motor Cortex ◽  
Inferior Frontal Gyrus ◽  
Voluntary Action ◽  
Button Press ◽  
Reactive Inhibition ◽  
Tic Suppression

Tourette syndrome is characterised by ‘unvoluntary’ tics, which are compulsive, yet often temporarily suppressible. The inferior frontal gyrus (IFG) is implicated in motor control, including inhibition of pre-potent actions through influences on downstream subcortical and motor regions. While tic suppression in Tourette Syndrome also engages the IFG, it is unclear whether such prefrontal control of action is also dysfunctional: Tic suppression studies do not permit comparison with control groups, and neuroimaging studies of motor inhibition can be confounded by the concurrent expression or suppression of tics. Here, patients with Tourette syndrome were directly compared to control participants when performing an intentional inhibition task during fMRI. Tic expression was recorded throughout for removal from statistical models. Participants were instructed to make a button press in response to Go cues, withheld responses to NoGo cues to, and decide whether to press or withhold to ‘Choose’ cues. Overall performance was similar between groups, for both intentional inhibition rates (% Choose-Go) and reactive NoGo inhibition commission errors. A subliminal face prime elicited no additional effects on intentional or reactive inhibition. Across participants, the task activated prefrontal and motor cortices and subcortical nuclei, including pre-supplementary motor area (preSMA), IFG, insula, caudate nucleus, thalamus, and primary motor cortex. In Tourette syndrome, activity was elevated in the IFG, insula, and basal ganglia, most notably within the right IFG during voluntary action and inhibition (Choose-Go and Choose-NoGo), and reactive inhibition (NoGo-correct). Anatomically, the locus of this IFG hyperactivation during control of voluntary action matched that previously reported for tic suppression. In Tourette syndrome, activity within the caudate nucleus was also enhanced during both intentional (Choose-NoGo) and reactive (NoGo-correct) inhibition. Strikingly, despite the absence of overt motor behaviour, primary motor cortex activity increased in patients with Tourette syndrome but decreased in controls during both reactive and intentional inhibition. Additionally, severity of premonitory sensations scaled with functional connectivity of the preSMA to the caudate nucleus, globus pallidus, and thalamus when choosing to respond (Choose-Go). Together, these results suggest that patients with Tourette syndrome use equivalent prefrontal mechanisms to suppress tics and withhold non-tic actions, but require greater IFG engagement than controls to overcome motor drive from hyperactive downstream regions, notably primary motor cortex. Moreover, premonitory sensations may cue midline motor regions to generate tics through interactions with the basal ganglia.

scholarly journals Anterograde Tracing From the Göttingen Minipig Motor and Prefrontal Cortex Displays a Topographic Subthalamic and Striatal Axonal Termination Pattern Comparable to Previous Findings in Primates

2021 ◽  
Vol 15 ◽  
Author(s):  
Johannes Bech Steinmüller ◽  
Carsten Reidies Bjarkam ◽  
Dariusz Orlowski ◽  
Jens Christian Hedemann Sørensen ◽  
Andreas Nørgaard Glud
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Prefrontal Cortex ◽  
Basal Ganglia ◽  
Motor Cortex ◽  
Caudate Nucleus ◽  
Subthalamic Nucleus ◽  
Primary Motor Cortex ◽  
Large Animal ◽  
Göttingen Minipig

Background: Deep brain stimulation (DBS) of the dorsal subthalamic nucleus (STN) is a validated neurosurgical treatment of Parkinson’s Disease (PD). To investigate the mechanism of action, including potential DBS induced neuroplasticity, we have previously used a minipig model of Parkinson’s Disease, although the basal ganglia circuitry was not elucidated in detail.Aim: To describe the cortical projections from the primary motor cortex (M1) to the basal ganglia and confirm the presence of a cortico-striatal pathway and a hyperdirect pathway to the subthalamic nucleus, respectively, which is known to exist in primates.Materials and Methods: Five female Göttingen minipigs were injected into the primary motor cortex (n = 4) and adjacent prefrontal cortex (n = 1) with the anterograde neuronal tracer, Biotinylated Dextran Amine (BDA). 4 weeks later the animals were sacrificed and the brains cryosectioned into 30 μm thick coronal sections for subsequent microscopic analysis.Results: The hyperdirect axonal connections from the primary motor cortex were seen to terminate in the dorsolateral STN, whereas the axonal projections from the prefrontal cortex terminated medially in the STN. Furthermore, striatal tracing from the motor cortex was especially prominent in the dorsolateral putamen and less so in the dorsolateral caudate nucleus. The prefrontal efferents were concentrated mainly in the caudate nucleus and to a smaller degree in the juxtacapsular dorsal putamen, but they were also found in the nucleus accumbens and ventral prefrontal cortex.Discussion: The organization of the Göttingen minipig basal ganglia circuitry is in accordance with previous descriptions in primates. The existence of a cortico-striatal and hyperdirect basal ganglia pathway in this non-primate, large animal model may accordingly permit further translational studies on STN-DBS induced neuroplasticity of major relevance for future DBS treatments.

Corticospinal Tract Microstructure Correlates With Beta Oscillatory Activity in the Primary Motor Cortex After Stroke

Stroke ◽  
2021 ◽  
Author(s):  
Robert Schulz ◽  
Marlene Bönstrup ◽  
Stephanie Guder ◽  
Jingchun Liu ◽  
Benedikt Frey ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Fractional Anisotropy ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Premotor Cortex ◽  
Motor Impairment ◽  
Motor Area ◽  
Oscillatory Activity ◽  
Premotor Area ◽  
Beta Power

Background and Purpose: Cortical beta oscillations are reported to serve as robust measures of the integrity of the human motor system. Their alterations after stroke, such as reduced movement-related beta desynchronization in the primary motor cortex, have been repeatedly related to the level of impairment. However, there is only little data whether such measures of brain function might directly relate to structural brain changes after stroke. Methods: This multimodal study investigated 18 well-recovered patients with stroke (mean age 65 years, 12 males) by means of task-related EEG and diffusion-weighted structural MRI 3 months after stroke. Beta power at rest and movement-related beta desynchronization was assessed in 3 key motor areas of the ipsilesional hemisphere that are the primary motor cortex (M1), the ventral premotor area and the supplementary motor area. Template trajectories of corticospinal tracts (CST) originating from M1, premotor cortex, and supplementary motor area were used to quantify the microstructural state of CST subcomponents. Linear mixed-effects analyses were used to relate tract-related mean fractional anisotropy to EEG measures. Results: In the present cohort, we detected statistically significant reductions in ipsilesional CST fractional anisotropy but no alterations in EEG measures when compared with healthy controls. However, in patients with stroke, there was a significant association between both beta power at rest ( P =0.002) and movement-related beta desynchronization ( P =0.003) in M1 and fractional anisotropy of the CST specifically originating from M1. Similar structure-function relationships were neither evident for ventral premotor area and supplementary motor area, particularly with respect to their CST subcomponents originating from premotor cortex and supplementary motor area, in patients with stroke nor in controls. Conclusions: These data suggest there might be a link connecting microstructure of the CST originating from M1 pyramidal neurons and beta oscillatory activity, measures which have already been related to motor impairment in patients with stroke by previous reports.

Comparison of Neural Activity in the Supplementary Motor Area and in the Primary Motor Cortex in Monkeys

1991 ◽  
Vol 8 (1) ◽  
pp. 27-44 ◽  
Author(s):  
Chen Dao-fen ◽  
B. Hyland ◽  
V. Maier ◽  
A. Palmeri ◽  
M. Wiesendanger
Keyword(s):  
Motor Cortex ◽  
Neural Activity ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Motor Area

scholarly journals The BOLD response in primary motor cortex and supplementary motor area during kinesthetic motor imagery based graded fMRI neurofeedback

NeuroImage ◽  
2019 ◽  
Vol 184 ◽  
pp. 36-44 ◽  
Author(s):  
David M.A. Mehler ◽  
Angharad N. Williams ◽  
Florian Krause ◽  
Michael Lührs ◽  
Richard G. Wise ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Motor Imagery ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Motor Area ◽  
Bold Response

Role of the Human Rostral Supplementary Motor Area and the Basal Ganglia in Motor Sequence Control: Investigations With H2 15O PET

1998 ◽  
Vol 79 (2) ◽  
pp. 1070-1080 ◽  
Author(s):  
H. Boecker ◽  
A. Dagher ◽  
A. O. Ceballos-Baumann ◽  
R. E. Passingham ◽  
M. Samuel ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Motor Area ◽  
Anterior Cingulate ◽  
Central Control ◽  
Motor Sequence ◽  
Finger Movements ◽  
Sequence Complexity

Boecker, H., A. Dagher, A. O. Ceballos-Baumann, R. E. Passingham, M. Samuel, K. J. Friston, J.-B. Poline, C. Dettmers, B. Conrad, and D. J. Brooks. Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. J. Neurophysiol. 79: 1070–1080, 1998. The aim of this study was to investigate the functional anatomy of distributed cortical and subcortical motor areas in the human brain that participate in the central control of overlearned complex sequential unimanual finger movements. On the basis of previous research in nonhuman primates, a principal involvement of basal ganglia (medial premotor loops) was predicted for central control of finger sequences performed automatically. In pertinent areas, a correlation of activation levels with the complexity of a motor sequence was hypothesized. H2 15O positron emission tomography (PET) was used in a group of seven healthy male volunteers [mean age 32.0 ± 10.4 yr] to determine brain regions where levels of regional cerebral blood flow (rCBF) correlated with graded complexity levels of five different key-press sequences. All sequences were overlearned before PET and involved key-presses of fingers II–V of the right hand. Movements of individual fingers were kept constant throughout all five conditions by external pacing at 1-Hz intervals. Positive correlations of rCBF with increasing sequence complexity were identified in the contralateral rostral supplementary motor area (pre-SMA) and the associated pallido-thalamic loop, as well as in right parietal area 7 and ipsilateral primary motor cortex (M1). In contrast, while rCBF in contralateral M1 and and extensive parts of caudal SMA was increased compared with rest during task performance, significant correlated increases of rCBF with sequence complexity were not observed. Inverse correlations of rCBF with increasing sequence complexity were identified in mesial prefrontal-, medial temporal-, and anterior cingulate areas. The findings provide further evidence in humans supporting the notion of a segregation of SMA into functionally distinct subcomponents: although pre-SMA was differentially activated depending on the complexity of a sequence of learned finger movements, such modulation was not detectable in caudal SMA (except the most antero-superior part), implicating a motor executive role. Our observations of complexity-correlated rCBF increases in anterior globus palllidus suggest a specific role for the basal ganglia in the process of sequence facilitation and control. They may act to filter and focus input from motor cortical areas as patterns of action become increasingly complex.

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