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Low- and high-threshold primary afferent inputs to spinal lamina III antenna-type neurons

Fernandes, Elisabete C.a,b; Santos, Ines C.a,b; Kokai, Evac,d,e; Luz, Liliana L.a,b; Szucs, Peterc,d,e; Safronov, Boris V.a,b,*

doi: 10.1097/j.pain.0000000000001320
Research Paper

The dorsal horn of the spinal cord (laminae I-VI) processes diverse modalities of nociceptive and nonnociceptive sensory information. Antenna-type neurons with cell bodies located in lamina III and large dendritic trees extending from the superficial lamina I to deep lamina IV are best shaped for the integration of a wide variety of inputs arising from primary afferent fibers and intrinsic spinal circuitries. Although the somatodendritic morphology, the hallmark of antenna neurons, has been well studied, little is still known about the axon structure and basic physiological properties of these cells. Here, we did whole-cell recordings in a rat (P9-P12) spinal cord preparation with attached dorsal roots to examine the axon course, intrinsic firing properties, and primary afferent inputs of antenna cells. Nine antenna cells were identified from a large sample of biocytin-filled lamina III neurons (n = 46). Axon of antenna cells showed intensive branching in laminae III-IV and, in half of the cases, issued dorsally directed collaterals reaching lamina I. Antenna cells exhibited tonic and rhythmic firing patterns; single spikes were followed by hyperpolarization or depolarization. The neurons received monosynaptic inputs from the low-threshold Aβ afferents, Aδ afferents, as well as from the high-threshold Aδ, and C afferents. When selectively activated, C-fiber-driven monosynaptic and polysynaptic excitatory postsynaptic potentials were sufficiently strong to evoke firing in the neurons. Thus, lamina III antenna neurons integrate low-threshold and nociceptive high-threshold primary afferent inputs and can function as wide dynamic range neurons able to directly connect deep dorsal horn with the major nociceptive projection area lamina I.

Antenna neurons integrate low- and high-threshold primary afferent inputs and can function as wide dynamic range neurons able to directly connect deep and superficial dorsal horns.

aInstituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal

bNeuronal Networks Group, Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Porto, Portugal

cMTA-DE-NAP B-Pain Control Research Group, Debrecen, Hungary

dMTA-DE Neuroscience Research Group, Debrecen, Hungary

eDepartment of Anatomy, Histology and Embryology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

Corresponding author. Address: Neuronal Networks Group, Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal. Tel.: 351-220408837. E-mail address: safronov@ibmc.up.pt (B.V. Safronov).

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

E.C. Fernandes, I.C. Santos and E. Kokai contributed equally to this work.

Received January 25, 2018

Received in revised form June 11, 2018

Accepted June 15, 2018

© 2018 International Association for the Study of Pain
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