Non-invasive brain stimulation as a tool to study cerebellar-M1 interactions in humans

Tremblay, Sara; Austin, Duncan; Hannah, Ricci; Rothwell, John C.

doi:10.1186/s40673-016-0057-z

Cerebellum & Ataxias

Table 5 Effect of cerebellum modulation on M1 neurophysiology assessed with TMS in healthy individuals

From: Non-invasive brain stimulation as a tool to study cerebellar-M1 interactions in humans

Outcome measure	Plasticity protocol	Authors	Parameters	Findings
1. Corticospinal excitability
Resting motor threshold	Anodal TDCS	Galea et al. (2009) [41]		↔
	Cathodal TDCS	Galea et al. (2009) [41]		↔
	1 Hz rTMS	Langguth et al. (2008) [47]		↔
	10 Hz rTMS	Langguth et al. (2008) [47]		↔
	cTBS	Di Lorenzo et al. (2013) [40]		↔
		Koch et al. (2008) [34]		↔
		Harrington et al. (2015) [39]		↔
	iTBS	Koch et al. (2008) [34]		↔
	iTBS	Harrington et al. (2015) [39]		↔
MEP amplitude	Anodal TDCS	Galea et al. (2009) [41]	1 mV	↔
	Cathodal TDCS	Galea et al. (2009) [41]	1 mV	↔
	TACS	Naro et al. (2016) [45]	120 % RMT	↑ contralateral up to 15 min (50 Hz)
	1 Hz rTMS	Gerschlager et al. (2002) [29]	1–1.5 mV	↑ up to 30 min
		Oliveri et al. (2005) [30]	1 mV	↑ contralateral up to 15 min ↔ ipsilateral
		Fierro et al (2007) [31]	120 % RMT	↔ 5–10 min ↑ 15–20 min
		Popa et al. (2010) [32]	120 % RMT	↔
	cTBS	Koch et al. (2008) [34]	1 mV	↓ up to 15 min
		Popa et al. (2010) [32]	120 % RMT	↔
		Di Lorenzo et al. (2013) [40]	1 mV	↔
		Li Voti et al. (2014) [35]	1 mV	↓ up to 30 min
		Di Biasio et al. (2014) [33]	120 % RMT	↓
		Carrillo et al. (2013) [36]	0.5–1 mV	↓ up to 40 min
		Harrington et al. (2015) [39]	110 % RMT	↓ (rest) ↔ (active)
	iTBS	Koch et al. (2008) [34]	1 mV	↑ up to 15 min
		Popa et al. (2010) [32]	120 % RMT	↔
		Harrington et al. (2015) [39]	110 % RMT	↔ (rest and active)
	CB-M1 PAS	Lu et al. (2012) [19]	1 mV	↑ (PAS_2ms) ↓ (PAS_6ms, PAS_10ms)
MEP recruitment curve	Anodal TDCS	Hamada et al. (2012) [42]	100, 120 and 140 % RMT	↔
	Anodal TDCS	Hamada et al. (2014) [44]	100, 120, 140 and 160 % RMT	↔ PA rest (online) ↔ AP rest (online) ↔ PA active (online) ↓ AP active (online)
	Cathodal TDCS	Galea et al. (2009) [41]	100, 110, 120, 130 and 140 % RMT	↔ (1 and 2 mA)
	Cathodal TDCS	Hamada et al. (2012) [42]	100, 120 and 140 % RMT	↔
	cTBS	Bologna et al. (2015) [38]	100 to 150 % RMT	↓ 5 min, return to baseline 45 min
	cTBS	Bologna et al. (2015b) [37]	100 to 140 % RMT	↓ up to 45 min
2. Cerebellum brain inhibition
CBI	Anodal TDCS	Galea et al. (2009) [41]	ISI: 5 ms CS: 5 % below bsAMT, and 5, 10, 15, 20, 25 % below bsAMT TS 1 mV (adjusted post)	↑ CBI recruitment curve at 20–25 % below bsAMT
	Anodal TDCS	Doeltgen et al. (2015) [46]	ISI: 5 ms CS: 100 % RMT (FDI) TS : 50 % MEP_MAX	↓
	Cathodal TDCS	Galea et al. (2009) [41]	ISI: 3 and 5 ms CS: 5 % below bsAMT TS: 1 mV (adjusted post)	↓ (2 mA only, until 30 min post-TDCS) ↔ no CBI at 3 ms ISI
	TACS	Naro et al. (2016) [45]	ISI: 7 ms CS: 90 % AMT TS: 120 % RMT	↓ (50 Hz: up to 15 min post-TACS) ↑ (300 Hz: only 0 min post-TACS)
	1 Hz rTMS	Popa et al. (2010) [32]	ISI: 5 ms CS: 90 % adjusted-RMT TS: 120 % RMT	↓ (contralateral only, until 30 min post)
	cTBS	Popa et al. (2010) [32]	ISI: 5 ms CS: 90 % adjusted-RMT TS: 120 % RMT	↓
	iTBS	Popa et al. (2010) [32]	ISI: 5 ms CS: 90 % adjusted-RMT TS: 120 % RMT	↔
	CB-M1 PAS	Lu et al. (2012) [19]	ISI: 7 ms CS: 95 % AMT (inion) TS: 0.6–0.8 mV (FDI)	↓
4. Intracortical inhibition
SICI	Anodal TDCS	Galea et al. (2009) [41]	ISI: 2 ms CS: 80 % RMT TS: 1 mV (adjusted post)	↔
	Cathodal TDCS	Galea et al. (2009) [41]	ISI: 2 ms CS: 80 % RMT TS: 1 mV (adjusted post)	↔
	1 Hz rTMS	Oliveri et al. (2005) [30]	ISI: 1 and 3 ms CS: 70 % RMT TS: 1 mV (adjusted post)	↔
		Fierro et al. (2007) [31]	ISI: 2 and 4 ms CS: 80 % RMT TS: 120 % RMT (adjusted post)	↔
		Langguth et al. (2008) [47]	ISI: 2, 3, 4 and 5 ms CS: 90 % AMT, TS: 1 mV	↑ (averaged ISIs)
	10 Hz rTMS	Langguth et al. (2008) [47]	ISI: 2, 3, 4 and 5 ms CS: 90 % AMT, TS: 1 mV	↔
	cTBS	Koch et al. (2008) [34]	ISI: 1, 2, 3, 4 and 5 ms CS: 80 % AMT, TS: 1 mV	↓ (3 ms, contralateral only)
		Carrillo et al. (2013) [36]	ISI: 1, 2, 3, 4 and 5 ms CS: 80 % AMT TS: 1 mV	↓ (2 and 3 ms, 0–20 min)
		Di Lorenzo et al. (2013) [40]	ISI: 1, 2, 3, 4 and 5 ms CS: 80 % AMT TS: 1 mV	↔
		Hubsch et al. (2013) [49]	SI: 2.5 ms CS: 70 % RMT TS: 130 % RMT (adjusted post)	↔
	iTBS	Koch et al. (2008) [34]	ISI: 1, 2, 3, 4 and 5 ms CS: 80 % AMT TS: 1 mV	↔
	CB-M1 PAS	Lu et al. (2012) [19]	ISI: 2 ms CS: 70 to 90 % AMT (50 % inh.)	↓ (all PAS ISIs)
LICI	TACS	Naro et al. (2016) [45]	ISI: 50 ms CS: 120 % RMT TS: 120 % RMT	↔
	cTBS	Koch et al. (2008) [34]	ISI: 100 and 150 ms CS: 120 % RMT TS: 1 mV	↑ (100 ms)
	cTBS	Hubsch et al. (2013) [49]	SI: 100 ms CS: 120 % RMT TS: 130 % RMT (adjusted post)	↔
	iTBS	Koch et al. (2008) [34]	ISI: 100 and 150 ms CS: 120 % RMT TS: 1 mV	↓ (100 ms)
CSP	1 Hz rTMS	Oliveri et al. (2005) [30]	30 % maximal force TS: 1 mV	↔
	cTBS	Harrington et al. (2015) [39]	20 Newton force TS:110 % RMT	↔
	iTBS	Harrington et al. (2015) [39]	20 Newton force TS:110 % RMT	↔
5. Intracortical facilitation
ICF	Anodal TDCS	Galea et al. (2009) [41]	ISI: 10 ms CS: 80 % RMT TS: 1 mV (adjusted post)	↔
	Cathodal TDCS	Galea et al. (2009) [41]	ISI: 10 ms CS: 80 % RMT TS: 1 mV (adjusted post)	↔
	1 Hz rTMS	Oliveri et al. (2005) [30]	ISI: 7, 10 and 15 ms CS: 70 % RMT TS: 1 mV (adjusted post)	↑ (15 ms)
		Fierro et al (2007) [31]	ISI: 7, 10 and 15 ms CS: 80 % RMT TS: 120 % RMT	↓ (10 ms)
		Langguth et al. (2008) [47]	ISI: 7, 8, 10, 15 and 20 ms CS: 90 % AMT TS: 1 mV	↑ (15 and 20 ms)
	10 Hz rTMS	Langguth et al. (2008) [47]	ISI: 7, 8, 10, 15 and 20 ms CS: 90 % AMT TS: 1 mV	↔
	iTBS	Koch et al. (2008) [34]	ISI: 7, 10 and 15 ms CS: 80 % AMT TS: 1 mV	↓ (15 ms)
	cTBS	Koch et al. (2008) [34]	ISI: 7, 10 and 15 ms CS: 80 % AMT TS: 1 mV	↔
		Carrillo et al. (2013) [36]	ISI: 7, 10 and 15 ms CS: 80 % AMT TS: 1 mV	↔
		Di Lorenzo et al. (2013) [40]	ISI: 7, 10 and 15 ms CS: 80 % AMT TS: 1 mV	↔
		Hubsch et al. (2013) [48]	SI: 15 ms CS: 70 % RMT TS: 130 % RMT (adjusted post)	↔
	CB-M1 PAS	Lu et al. (2012) [19]	ISI: 10 ms CS: 70 to 95 % AMT	↔
SICF	cTBS	Koch et al. (2008) [34]	ISI: 1.0, 1.3, 2.1, 2.5, 3.3, 4.1 ms CS: 90 % RMT TS: 130 % RMT	↔
SICF	iTBS	Koch et al. (2008) [34]	ISI: 1.0, 1.3, 2.1, 2.5, 3.3, 4.1 ms CS: 90 % RMT TS: 130 % RMT	↔
6. Afferent inhibition
SAI	Anodal TDCS	Hamada et al. (2012) [42]	ISI: 15, 20 and 25 ms TS: 1 mV	↔
	Anodal TDCS	Doeltgen et al. (2015) [46]	ISI: 25 and 30 ms TS : 50 % MEP_MAX	↔
	Cathodal TDCS	Hamada et al. (2012) [42]	ISI: 15, 20 and 25 ms TS: 1 mV	↔
	cTBS	Di Lorenzo et al. (2013) [40]	ISI: N20 – 4 ms to N20 + 8 ms TS: 1 mV	↔
	cTBS	Hubsch et al. (2013) [49]	ISI: 20 ms TS: 130 % RMT (adjusted post) CS: 130 % sensory threshold	↔
SAI recruitment curve	cTBS	Di Lorenzo et al. (2013) [40]	ISI: N20 – 4 ms to N20 + 8 ms TS: 1 mV CS: 100, 200 and 300 % sensory threshold	↔
LAI	cTBS	Hubsch et al. (2013) [49]	ISI: 200 ms TS: 130 % RMT (adjusted post) CS: 130 % sensory threshold	↔
7. Motor cortex plasticity
PAS	Anodal TDCS	Hamada et al. (2012) [42]	ISI: 21.5 and 25 ms	↓ PAS₂₅ ↔ PAS_21.5
		Hamada et al. (2014) [44]	ISI: 21.5 and 25 ms	↓ PAS₂₅ ↔ PAS_21.5
		Strigaro et al. (2014) [52]	ISI: 21.5, 25 ms and variable	↑ PAS_var
	Cathodal TDCS	Hamada et al. (2012) [42]	ISI: 21.5 and 25 ms	↓ PAS₂₅
	cTBS	Popa et al. (2013) [50]	ISI: 25 ms	↑ PAS₂₅ (post 25–60 min)
	cTBS	Hubsch et al. (2013) [49]	ISI: 25 ms	↑ PAS₂₅
		Kishore et al. (2014) [51]	ISI: 25 ms	↔ PAS₂₅
	iTBS	Popa et al. (2013) [50]	ISI: 25 ms	↓ PAS₂₅ (post 5–15 min)
	iTBS	Hubsch et al. (2013) [49]	ISI: 25 ms	↓PAS₂₅
cTBS	iTBS	Popa et al. (2013) [50]	80 % AMT, 600 pulses Contra. M1	↔
iTBS	iTBS	Popa et al. (2013) [50]	80 % AMT, 600 pulses Contra. M1	↔

AMT active motor threshold, CBI cerebellar brain inhibition, CS conditioning stimulus, Contra contralateral, CSP cortical silent period, HC healthy controls, ICF intracortical facilitation, Ipsi. ipsilateral, ISI inter-stimulus interval, LAI long latency afferent inhibition, LICI long interval intracortical inhibition, MEP motor evoked potential, PAS paired-associative stimulation, SAI short latency afferent inhibition, SICI short interval intracortical inhibition, SICF short interval intracortical facilitation, TS test stimulus

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