Distinct mechanisms of signal processing by lamina I spino-parabrachial neurons

K Agashkov,Y Andrianov,M Krasniakova,Y Zabenko,N Voitenko,D Shevchuk,B V Safronov,P Belan,V Krotov

doi:10.1038/s41598-019-55462-7

K Agashkov, Y Andrianov + Show 7 more

Open Access

https://doi.org/10.1038/s41598-019-55462-7

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Abstract

Lamina I spino-parabrachial neurons (SPNs) receive peripheral nociceptive input, process it and transmit to the supraspinal centres. Although responses of SPNs to cutaneous receptive field stimulations have been intensively studied, the mechanisms of signal processing in these neurons are poorly understood. Therefore, we used an ex-vivo spinal cord preparation to examine synaptic and cellular mechanisms determining specific input-output characteristics of the neurons. The vast majority of the SPNs received a few direct nociceptive C-fiber inputs and generated one spike in response to saturating afferent stimulation, thus functioning as simple transducers of painful stimulus. However, 69% of afferent stimulation-induced action potentials in the entire SPN population originated from a small fraction (19%) of high-output neurons. These neurons received a larger number of direct Aδ- and C-fiber inputs, generated intrinsic bursts and efficiently integrated a local network activity via NMDA-receptor-dependent mechanisms. The high-output SPNs amplified and integrated the nociceptive input gradually encoding its intensity into the number of generated spikes. Thus, different mechanisms of signal processing allow lamina I SPNs to play distinct roles in nociception.

Highlights

Lamina I spino-parabrachial neurons (SPNs) receive peripheral nociceptive input, process it and transmit to the supraspinal centres
Www.nature.com/scientificreports illumination; epifluorescent and infrared light-emitting-diode (IR-LED) images of a retrogradely labelled SPN. (Ca–c), characteristic discharges evoked by the saturating dorsal root stimulation (1 ms, 140 μA) in a low-output SPN (LO-SPN), a medium-output SPN (MO-SPN) and high-output SPNs (HO-SPNs)
And in the following figures, the time moments of the stimulations are indicated by arrows. (Da), the histogram showing distribution of SPNs according to the number of spikes evoked by the dorsal root stimulation. (Db), a total number of spikes evoked in the populations of LO, MO- and HO-SPNs by the saturating dorsal root stimulation

Summary

Introduction

Lamina I spino-parabrachial neurons (SPNs) receive peripheral nociceptive input, process it and transmit to the supraspinal centres. 69% of afferent stimulation-induced action potentials in the entire SPN population originated from a small fraction (19%) of high-output neurons These neurons received a larger number of direct Aδ- and C-fiber inputs, generated intrinsic bursts and efficiently integrated a local network activity via NMDAreceptor-dependent mechanisms. We revealed distinct groups of SPNs according to their input-output characteristics, which were determined by specific combinations of intrinsic firing properties, primary afferent inputs and degree of interaction with a local neuronal circuitry These mechanisms were found to play a crucial role in the output signal encoding by SPNs. our study revealed synaptic and cellular mechanisms, which allow lamina I SPNs to play different roles in processing of nociceptive information

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