State-dependent and timing-dependent bidirectional associative plasticity in the human SMA-M1 network.
The supplementary motor area (SMA-proper) plays a key role in the preparation and execution of voluntary movements. Anatomically, SMA-proper is densely reciprocally connected to primary motor cortex (M1), but neuronal coordination within the SMA-M1 network and its modification by external perturbation are not well understood. Here we modulated the SMA-M1 network using MR-navigated multicoil associative transcranial magnetic stimulation in healthy subjects. Changes in corticospinal excitability were assessed by recording motor evoked potential (MEP) amplitude bilaterally in a hand muscle. We found timing-dependent bidirectional Hebbian-like MEP changes during and for at least 30 min after paired associative SMA-M1 stimulation. MEP amplitude increased if SMA stimulation preceded M1 stimulation by 6 ms, but decreased if SMA stimulation lagged M1 stimulation by 15 ms. This associative plasticity in the SMA-M1 network was highly topographically specific because paired associative stimulation of pre-SMA and M1 did not result in any significant MEP change. Furthermore, associative plasticity in the SMA-M1 network was strongly state-dependent because it required priming by near-simultaneous M1 stimulation to occur. We conclude that timing-dependent bidirectional associative plasticity is demonstrated for the first time at the systems level of a human corticocortical neuronal network. The properties of this form of plasticity are fully compatible with spike-timing-dependent plasticity as defined at the cellular level. The necessity of priming may reflect the strong interhemispheric connectivity of the SMA-M1 network. Findings are relevant for better understanding reorganization and potentially therapeutic modification of neuronal coordination in the SMA-M1 network after cerebral lesions such as stroke.
Department of Neurology, Goethe-University Frankfurt, 60528 Frankfurt am Main, Germany.
Noritoshi
N
Arai
Florian
F
Müller-Dahlhaus
Takenobu
T
Murakami
Barbara
B
Bliem
Ming-Kuei
MK
Lu
Yoshikazu
Y
Ugawa
Ulf
U
Ziemann
D000328:Adult; D000704:Analysis of Variance; D001703:Biophysics; D004576:Electromyography / Q000379:methods; D019054:Evoked Potentials, Motor / Q000502:physiology*; D005260:Female; D007839:Functional Laterality; D006801:Humans; D008297:Male; D009044:Motor Cortex / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D011930:Reaction Time / Q000502:physiology; D013997:Time Factors; D050781:Transcranial Magnetic Stimulation; D055815:Young Adult