Adaptive changes in the neuromagnetic response of the primary and association somatosensory areas following repetitive tactile hand stimulation in humans

Abstract

Cortical adaptation in the primary somatosensory cortex (SI) has been probed using different stimulation modalities and recording techniques, in both human and animal studies. In contrast, considerably less knowledge has been gained about the adaptation profiles in other areas of the cortical somatosensory network. Using magnetoencephalography, we examined the patterns of short-term adaptation for evoked responses in SI and somatosensory association areas during tactile stimulation applied to the glabrous skin of the right hand. Cutaneous stimuli were delivered as trains of serial pulses with a constant frequency of 2 Hz and 4 Hz in separate runs, and a constant inter-train interval of 5 s. The unilateral stimuli elicited transient responses to the serial pulses in the train, with several response components that were separated by Independent Component Analysis. Subsequent neuromagnetic source reconstruction identified regional generators in the contralateral SI and somatosensory association areas in the posterior parietal cortex (PPC). Activity in the bilateral secondary somatosensory cortex (i.e. SII/PV) was also identified, although less consistently across subjects. The dynamics of the evoked activity in each area and the frequency-dependent adaptation effects were assessed from the changes in the relative amplitude of serial responses in each train. We show that the adaptation profiles in SI and PPC can be quantitatively characterized from neuromagnetic recordings using tactile stimulation, with the sensitivity to repetitive stimulation increasing from SI to PPC. A similar approach for SII/PV has proven less straightforward, potentially due to the selective nature of these areas to respond predominantly to certain stimuli.

Neural encoding of saltatory pneumotactile velocity in human glabrous hand

“…Overall, the BOLD main effect for saltatory pneumotactile velocity was localized to several loci involving contralateral and bilateral cerebral cortex, and ipsilateral cerebellum. This elaborate network extends previous observations based on fMRI and MEG of pneumotactile encoding of single channel pulse train inputs (non-saltatory) which found principal dipoles localized to S1, S2 and PPC in both contralateral and bilateral cerebral sensorimotor cortex [ 52 , 53 ]. Additionally, the cerebral responses in S1 and PPC are generally consistent with the findings from our previous MEG studies using the first and second generation of TAC-Cells (19.3 mm ID, and 6 mm ID, respectively) developed in our laboratory [ 43 , 44 , 53 ].…”

“…This elaborate network extends previous observations based on fMRI and MEG of pneumotactile encoding of single channel pulse train inputs (non-saltatory) which found principal dipoles localized to S1, S2 and PPC in both contralateral and bilateral cerebral sensorimotor cortex [ 52 , 53 ]. Additionally, the cerebral responses in S1 and PPC are generally consistent with the findings from our previous MEG studies using the first and second generation of TAC-Cells (19.3 mm ID, and 6 mm ID, respectively) developed in our laboratory [ 43 , 44 , 53 ]. We also found significant ipsilateral BOLD responses in deep cerebellum which was reported in previous fMRI and PET studies using the brush and the foam-tipped motor to create the movement of the tactile stimulus (tickling) on the palm [ 17 , 19 , 54 ].…”

Brain encoding of saltatory velocity through a pulsed pneumotactile array in the lower face

“…The pneumotactile stimulator in the present study (GALILEO Somatosensory TM ) uses a chambered tactile cell (TAC-Cell) which can be applied quickly to the skin of any population using double adhesive tape collars, with scalable and programmable control to create saltatory tactile arrays unique to study designs. Recent studies utilizing pulse trains of pneumotactile stimulation at different stimulus rates (2-6 Hz) with just a single TAC-Cell placed on either the glabrous hand or lower face have shown significant and unique short-and long-term adaptation patterns in S1, S2, and posterior parietal cortex (PPC) using magnetoencephalography source localization methods (Popescu et al, , 2013Venkatesan et al, 2010Venkatesan et al, , 2014, and electroencephalography (Custead et al, 2015).…”

Adaptation of cortical activity to sustained pressure stimulation on the fingertip

“…An optical intrinsic imaging study in non-human primate has demonstrated changes in cortical activation with a decrease in the spatial extent of the responses of the primary somatosensory cortex (SI) during sustained vibrotactile stimulation (25 Hz) [ 4 ]. Recent human magnetoencephalography (MEG) (2 and 4 Hz) [ 5 ] and functional magnetic resonance imaging (fMRI) (18–26 Hz) [ 6 ] studies have reported that activities of the somatosensory and parietal cortical regions decreased over time during repetitive vibrotactile stimuli. However, to our knowledge, no human study has explored tactile adaptation at the cortical level to sustained pressure stimulation, which would be manifested in exponential decreases in cortical activation.…”