Cerebellar theta burst stimulation modulates the neural activity of interconnected parietal and motor areas

Casula, Elias Paolo; Pellicciari, Maria Concetta; Ponzo, Viviana; Bassi, Mario Stampanoni; Veniero, Domenica; Caltagirone, Carlo; Koch, Giacomo

doi:10.1038/srep36191

Cited by 96 publications

(108 citation statements)

References 47 publications

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“…Studies have reported N100 to be associated with GABA B -mediated inhibitory mechanisms in both motor (Bonnard et al, 2009;Farzan et al, 2013;Premoli, Rivolta, et al, 2014b;Rogasch, Daskalakis, et al, 2013a) and prefrontal cortex (Chung et al, 2017;Rogasch et al, 2015). The amplitude of N100 increased following SAI both in motor and prefrontal cortex (Noda et al, 2016;Noda, Zomorrodi, Backhouse, et al, 2017c), but decreased following cerebellar iTBS (Casula, Pellicciari, Ponzo, et al, 2016b), which are in line with the change observed in N100 following Ind iTBS. However, our previous studies showed increased N100 following prefrontal iTBS (50 Hz at 5 Hz) (Chung et al, 2017;Chung, Rogasch, Hoy, & Fitzgerald, 2018a;Chung, Rogasch, Hoy, Sullivan, et al, 2018b), and the discrepancy of the outcome…”

Section: Effect Of Individualised Itbs On Plastic Effects In the Prsupporting

confidence: 77%

“…It is interesting to note that cerebellar iTBS resulted in the opposite changes in N100 in two separate studies using 50 Hz (Casula, Pellicciari, Ponzo, et al, 2016b) and It is interesting to note that cerebellar iTBS resulted in the opposite changes in N100 in two separate studies using 50 Hz (Casula, Pellicciari, Ponzo, et al, 2016b) and…”

Section: Inter-individual Variability In the Response To Conventionmentioning

confidence: 97%

“…Characterisation of P200 is needed to better understand its role, as the changes in this component are often observed following neuromodulation (Casula, Pellicciari, Ponzo, et al, 2016b;Chung et al, 2017;Noda et al, 2016) or in clinical populations (Noda, Barr, Zomorrodi, Cash, Rajji, et al, 2017b). Positive correlations were observed only between mood and neurophysiological measures that showed the greatest change (i.e., Δ P60 at T5, Δ N100 at T30), suggesting robust physiological changes are required to translate into a behavioural outcome.…”

Section: Relationship Between Neurophysiological Changes and The Chmentioning

confidence: 99%

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The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

Chung

Sullivan

Rogasch

et al. 2018

Human Brain Mapping

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Recent studies have highlighted variability in response to theta burst stimulation (TBS) in humans. TBS paradigm was originally developed in rodents to mimic gamma bursts coupled with theta rhythms, and was shown to elicit long‐term potentiation. The protocol was subsequently adapted for humans using standardised frequencies of stimulation. However, each individual has different rhythmic firing pattern. The present study sought to explore whether individualised intermittent TBS (Ind iTBS) could outperform the effects of two other iTBS variants. Twenty healthy volunteers received iTBS over left prefrontal cortex using 30 Hz at 6 Hz, 50 Hz at 5 Hz, or individualised frequency in separate sessions. Ind iTBS was determined using theta‐gamma coupling during the 3‐back task. Concurrent use of transcranial magnetic stimulation and electroencephalography (TMS‐EEG) was used to track changes in cortical plasticity. We also utilised mood ratings using a visual analogue scale and assessed working memory via the 3‐back task before and after stimulation. No group‐level effect was observed following either 30 or 50 Hz iTBS in TMS‐EEG. Ind iTBS significantly increased the amplitude of the TMS‐evoked P60, and decreased N100 and P200 amplitudes. A significant positive correlation between neurophysiological change and change in mood rating was also observed. Improved accuracy in the 3‐back task was observed following both 50 Hz and Ind iTBS conditions. These findings highlight the critical importance of frequency in the parameter space of iTBS. Tailored stimulation parameters appear more efficacious than standard paradigms in neurophysiological and mood changes. This novel approach presents a promising option and benefits may extend to clinical applications.

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Section: Effect Of Individualised Itbs On Plastic Effects In the Prsupporting

confidence: 77%

Section: Inter-individual Variability In the Response To Conventionmentioning

confidence: 97%

Section: Relationship Between Neurophysiological Changes and The Chmentioning

confidence: 99%

See 1 more Smart Citation

The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

Chung

Sullivan

Rogasch

et al. 2018

Human Brain Mapping

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“…This modular organization means that TBS stimulation to different subregions will result in similar effects across distinct networks (Farzan 2016). Indeed, there has been investigation within the motor system of the effect of TBS, which is consistent with iTBS resulting in a change in distal motor cortex plasticity (Casula et al 2016; Koch et al 2008; Grimaldi et al, 2014). In the motor system, the cerebellum may contain an internal model predicting the course of future events based on past experience (Manto et al, 2012).…”

Section: Discussionmentioning

confidence: 65%

“…These parameters might have led to these opposite effects, as would be predicted by our network model of the stimulation effects (Halko et al, 2014). Others have reported reaction time changes and motor physiological changes from the application of TBS to the cerebellum, typically 1cm inferior and 3cm lateral to the inion (Koch et al, 2008, 2009; Picazio et al, 2016; Casula et al 2016). These motor sites are substantially superior and lateral to the typical dorsal attention network site.…”

Section: Discussionmentioning

confidence: 99%

Network-targeted cerebellar transcranial magnetic stimulation improves attentional control

et al. 2017

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Developing non-invasive brain stimulation interventions to improve attentional control is extremely relevant to a variety of neurologic and psychiatric populations, yet few studies have identified reliable biomarkers that can be readily modified to improve attentional control. One potential biomarker of attention is functional connectivity in the core cortical network supporting attention - the dorsal attention network (DAN). We used a network-targeted cerebellar transcranial magnetic stimulation (TMS) procedure, intended to enhance cortical functional connectivity in the DAN. Specifically, in healthy young adults we administered intermittent theta burst TMS (iTBS) to the midline cerebellar node of the DAN and, as a control, the right cerebellar node of the default mode network (DMN). These cerebellar targets were localized using individual resting-state fMRI scans. Participants completed assessments of both sustained (gradual onset continuous performance task, gradCPT) and transient attentional control (attentional blink) immediately before and after stimulation, in two sessions (cerebellar DAN and DMN). Following cerebellar DAN stimulation, participants had significantly fewer attentional lapses (lower commission error rates) on the gradCPT. In contrast, stimulation to the cerebellar DMN did not affect gradCPT performance. Further, in the DAN condition, individuals with worse baseline gradCPT performance showed the greatest enhancement in gradCPT performance. These results suggest that temporarily increasing functional connectivity in the DAN via network-targeted cerebellar stimulation can enhance sustained attention, particularly in those with poor baseline performance. With regard to transient attention, TMS stimulation improved attentional blink performance across both stimulation sites, suggesting increasing functional connectivity in both networks can enhance this aspect of attention. These findings have important implications for intervention applications of TMS and theoretical models of functional connectivity.

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Effect of Cerebellar Stimulation on Gait and Balance Recovery in Patients With Hemiparetic Stroke

et al. 2019

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IMPORTANCE Gait and balance impairment is associated with poorer functional recovery after stroke. The cerebellum is known to be strongly implicated in the functional reorganization of motor networks in patients with stroke, especially for gait and balance functions. OBJECTIVE To determine whether cerebellar intermittent θ-burst stimulation (CRB-iTBS) can improve balance and gait functions in patients with hemiparesis due to stroke. DESIGN, SETTING, PARTICIPANTS This randomized, double-blind, sham-controlled phase IIa trial investigated efficacy and safety of a 3-week treatment of CRB-iTBS coupled with physiotherapy in promoting gait and balance recovery in patients with stroke. Thirty-six patients with consecutive ischemic chronic stroke in the territory of the contralateral middle cerebral artery with hemiparesis were recruited from a neuro-rehabilitation hospital. Participants were screened and enrolled from March 2013 to June 2017. Intention-to-treat analysis was performed.INTERVENTIONS Patients were randomly assigned to treatment with CRB-iTBS or sham iTBS applied over the cerebellar hemisphere ipsilateral to the affected body side immediately before physiotherapy daily during 3 weeks. MAIN OUTCOMES AND MEASURESThe primary outcome was the between-group difference in change from baseline in the Berg Balance Scale. Secondary exploratory measures included the between-group difference in change from baseline in Fugl-Meyer Assessment scale, Barthel Index, and locomotion assessment with gait analysis and cortical activity measured by transcranial magnetic stimulation in combination with electroencephalogram. RESULTSA total of 34 patients (mean [SD] age, 64 [11.3] years; 13 women [38.2%]) completed the study. Patients treated with CRB-iTBS, but not with sham iTBS, showed an improvement of gait and balance functions, as revealed by a pronounced increase in the mean (SE) Berg Balance Scale score (baseline: 34.5 [3.4]; 3 weeks after treatment: 43.4 [2.6]; 3 weeks after the end of treatment: 47.5 [1.8]; P < .001). No overall treatment-associated differences were noted in the Fugl-Meyer Assessment (mean [SE], baseline: 163.8 [6.8]; 3 weeks after treatment: 171.1 [7.2]; 3 weeks after the end of treatment: 173.5 [6.9]; P > .05) and Barthel Index scores (mean [SE], baseline: 71.1 [4.92]; 3 weeks after treatment: 88.8 [2.1]; 3 weeks after the end of treatment: 92.2 [2.4]; P > .05). Patients treated with CRB-iTBS, but not sham iTBS, showed a reduction of step width at the gait analysis (mean [SE], baseline: 16.8 [4.8] cm; 3 weeks after treatment: 14.3 [6.2] cm; P < .05) and an increase of neural activity over the posterior parietal cortex.CONCLUSIONS AND RELEVANCE Cerebellar intermittent θ-burst stimulation promotes gait and balance recovery in patients with stroke by acting on cerebello-cortical plasticity. These results are important to increase the level of independent walking and reduce the risk of falling.

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Cerebellar theta burst stimulation modulates the neural activity of interconnected parietal and motor areas

Cited by 96 publications

References 47 publications

The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

Network-targeted cerebellar transcranial magnetic stimulation improves attentional control

Effect of Cerebellar Stimulation on Gait and Balance Recovery in Patients With Hemiparetic Stroke

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