Excitability modulations of somatosensory perception do not depend on feedforward neuronal population spikes.

Neural states shape perception at earliest cortical processing levels. Previous work in humans showed a relationship between initial cortical excitation, as indicated by the N20 component of the somatosensory evoked potential (SEP), pre-stimulus alpha oscillations, and the perceived intensity in a somatosensory discrimination paradigm. Here we address the follow-up question whether these excitability dynamics reflect changes in feedforward or feedback signals. To distinguish feedforward neural signals from feedback signals, we leveraged high-frequency oscillations (HFO) which have previously been shown to correspond to neuronal population spiking activity of the first excitatory feedforward volley in the somatosensory cortex. We examined these HFO in electroencephalography (EEG) data of 32 male human participants, performing a somatosensory intensity discrimination task. Spatial filtering and time-frequency analyses allowed to clearly distinguish HFO from the lower-frequency, conventional SEP. Using Bayesian statistics, we found evidence against the involvement of HFO in moment-to-moment variability of perceived stimulus intensity, in contrast to previously observed pre-stimulus alpha and N20 effects of the conventional SEP. Given that the N20 component presumably reflects backpropagating membrane potentials towards the apical dendrites (distal dendritic sites), we argue that top-down feedback processes (e.g., related to alpha oscillations) may thus rely on activity modulations at those distal dendrites of involved pyramidal cells rather than on synchronous output firing changes at their basal compartments.Significance Statement In the current work, we report evidence against the involvement of feedforward neuronal population spikes (non-invasively assessed by high-frequency oscillations, HFO) in moment-to-moment variability of the perceived intensity of somatosensory stimuli. Given that behaviorally relevant modulations of both pre-stimulus alpha activity and N20 amplitudes of the SEP were found in previous analyses of the same dataset, we suggest that these discrepancies can be explained by top-down excitability changes that act on apical rather than basal dendritic compartments. Thus, not the output of the first feedforward sweep seems to be affected by instantaneous neural states in somatosensory processing but rather its backpropagating counterpart in form of post-synaptic potentials in soma-dendritic direction.