Spinal processing of spatiotemporally diverse tactile stimuli: Implications for allodynia and spinal cord stimulation

Touch is mistakenly perceived as painful when inhibition in the spinal dorsal horn (SDH) is weakened. Disinhibition un-gates a polysynaptic spinal circuit but why mechanical allodynia is predominantly evoked by certain stimuli, like dynamic brushing, remains unclear. To answer this, we incorporated receptive fields (RFs) into a computational model of the SDH to study the processing of stimuli with different spatiotemporal features. Broad stimuli normally suppress output spiking by engaging inhibition from the RF surround, but the efficacy of inhibition depends on the input’s temporal pattern. This is critical since excitatory and inhibitory spinal neurons are preferentially sensitive to synchronous and asynchronous input, respectively. Furthermore, spikes driven by synchronous input are resistant to feedforward inhibition. The combined results explain why broad dynamic touch (e.g. brush or vibration) evokes more allodynia than punctate static touch. Our results also show that asynchronous and spatially disordered input evoked by kilohertz-frequency spinal cord stimulation preferentially activates inhibitory neurons, thus explaining its anti-allodynic effects.