Influence of cholinergic circuitries in generation of high-frequency somatosensory evoked potentials

• Published in: Clinical neurophysiology 2003-08, Vol.114 (8), p.1538-1548
• Main Authors: Restuccia, D, Marca, G.Della, Valeriani, M, Rubino, M, Paciello, N, Vollono, C, Capuano, A, Tonali, P
• Format: Article
• Language: English
• Subjects: 600 Hz bursts; Acetylcholine; Acetylcholine - physiology; Adult; Biological and medical sciences; Brain Mapping; Carbamates - pharmacology; Cerebral Cortex - drug effects; Cerebral Cortex - physiology; Chattering cells; Cholinesterase Inhibitors - pharmacology; Electric Stimulation; Electroencephalography; Evoked Potentials, Somatosensory - drug effects; Fundamental and applied biological sciences. Psychology; High-frequency oscillations; Humans; Male; Median Nerve - drug effects; Median Nerve - physiology; Neural Pathways; Phenylcarbamates; Reaction Time; Rivastigmine; Scalp; Somatosensory cortex; Somatosensory Cortex - drug effects; Somatosensory Cortex - physiology; Somatosensory evoked potentials; Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors; Vertebrates: nervous system and sense organs
• ISSN: 1388-2457; 1872-8952
• DOI: 10.1016/S1388-2457(03)00138-X

Objective: High-frequency oscillations (HFOs) evoked by upper limb stimulation reflect highly synchronised spikes generated in the somatosensory human system. Since acetylcholine produces differential modulation in subgroups of neurons, we would determine whether cholinergic drive influences HFOs. Methods: We recorded somatosensory evoked potentials (SEPs) from 31 scalp electrodes in 7 healthy volunteers, before and after single administration of rivastigmine, an inhibitor of central acetylcholinesterase. Right median nerve SEPs have been analysed after digital narrow bandpass filtering (500–700 Hz). Raw data were further submitted to Brain Electrical Source analysis (BESA) to evaluate the respective contribution of lemniscal, thalamic and cortical sources. Lastly, we analysed by Fast Fourier transform spectral changes after drug administration in the 10–30 ms latency range. Results: Rivastigmine administration caused a significant increase of HFOs in the 18–28 ms latency range. Wavelets occurring before the onset latency of the conventional N20 SEP did not show any significant change. A similar increase concerned the strength of cortical dipolar sources in our BESA model. Lastly, we found a significant power increase of the frequency peak at about 600 Hz in P3-F3 traces after drug intake. Conclusions: Our findings demonstrate that the cortical component of HFOs is significantly enhanced by cholinergic activation. Pyramidal chattering cells, which are capable to discharge high-frequency bursts, are mainly modulated by cholinergic inputs; by contrast, acetylcholine does not modify the firing rate of fast-spiking GABAergic interneurons. We thus discuss the hypothesis that cortical HFOs are mainly generated by specialised pyramidal cells.