Abstract

The induction of synaptic plasticity requires the presence of temporally patterned neural activity. Numerous cellular studies in animals and brain slices have demonstrated that long-term potentiation (LTP) enhances synaptic transmission, which can be evoked by high-frequency intermittent stimulation. In humans, plasticity processes underlying perceptual learning can be reliably induced by repetitive, LTP-like sensory stimulation. These protocols lead to improvement of perceptual abilities parallel to widespread remodeling of cortical processing. However, whether maintained rhythmic cortical activation induced by the LTP-like stimulation is also present during human perceptual learning experiments, remains elusive. To address this question, we here applied a 20 Hz intermittent stimulation protocol for 40 min to the index-, middle- and ring-fingers of the right hand, while continuously recording EEG over the hand representation in primary somatosensory cortex in young adult participants. We find that each train of stimulation initiates a transient series of sensory-evoked potentials which accumulate after about 500 ms into a 20 Hz steady-state response persisting over the entire period of the 2-s-train. During the inter-train interval, no consistent evoked activity can be detected. This response behavior is maintained over the whole 40 min of stimulation without any indication of habituation. However, the early stimulation evoked potentials (SEPs) and the event-related desynchronization (ERD) during the steady-state response change over the 40 min of stimulation. In a second experiment, we demonstrate in a separate cohort of participants that the here-applied pneumatic type of stimulation results in improvement of tactile acuity as typically observed for electrically applied 20 Hz intermittent stimulation. Our data demonstrate that repetitive stimulation using a 20 Hz protocol drives rhythmic activation in the hand representation of somatosensory cortex, which is sustained during the entire stimulation period. At the same time, cortical excitability increases as indicated by altered ERD and SEP amplitudes. Our results, together with previous data underlining the dependence of repetitive sensory stimulation effects on NMDA-receptor activation, support the view that repetitive sensory stimulation elicits LTP-like processes in the cortex, thereby facilitating perceptual learning processes.

Highlights

  • Under everyday-live conditions, humans learn largely through practicing and repetition

  • We found that 20 Hz stimulation of the skin evoked a reliable steady-state response at 20 Hz with no indication of habituation over the range of 40 min, while sensory evoked potentials (SEPs) and event-related desynchronization (ERD) changed over time

  • Grand average sensory evoked potentials recorded during 40 min repetitive intermittent 20 Hz stimulation of the fingertips, display clearly discernible components: P1 (2.1 μV ± 0.47), N1 (0.3 μV ± 0.26), P2 (1.43 μV ± 0.87), N2 (−0.31 μV ± 0.65), and P3 (4.84 μV ± 0.62)

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Summary

Introduction

Under everyday-live conditions, humans learn largely through practicing and repetition. Tactile acuity of the fingers is improved or decreased by mere exposure to stimulation, a process unaffected by confounding factors like attention or motivation (Godde et al, 2000; Ragert et al, 2008). To explain these behavioral effects, this specific form of stimulation was suggested to evoke synaptic plasticity processes in the cortical regions representing the stimulated skin sites (Pleger et al, 2001, 2003; Dinse et al, 2003). It has been shown that the efficacy of repetitive sensory stimulation protocols depends on NMDA-receptor activation (Dinse et al, 2003)

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