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Trigeminal Aδ- and C-afferent supply of lamina I neurons in the trigeminocervical complex

Luz, Liliana L.a,b; Fernandes, Elisabete C.a,b; Dora, Fannic,d; Lukoyanov, Nikolay V.a,b; Szucs, Peterc,d,e; Safronov, Boris V.a,b,*

doi: 10.1097/j.pain.0000000000001659
Research Paper

Nociceptive trigeminal afferents innervating craniofacial area, eg, facial skin and cranial meninges, project to a broad region in the medullary and upper cervical dorsal horn designated as the trigeminocervical complex. Lamina I neurons in the trigeminocervical complex integrate and relay peripheral inputs, thus playing a key role in both cranial nociception and primary headache syndromes. Because of the technically challenging nature of recording, the long-range trigeminal afferent inputs to the medullary and cervical lamina I neurons were not intensively studied so far. Therefore, we have developed an ex vivo brainstem–cervical cord preparation with attached trigeminal nerve for the visually guided whole-cell recordings from the medullary and cervical lamina I neurons. Two-thirds of recorded neurons generated intrinsic rhythmic discharges. The stimulation of the trigeminal nerve produced a complex effect; it interrupted the rhythmic discharge for hundreds of milliseconds but, if the neuron was silenced by a hyperpolarizing current injection, could elicit a discharge. The monosynaptic inputs from the trigeminal Aδ, high-threshold Aδ, low-threshold C, and C afferents were recorded in the medullary neurons, as well as in the cervical neurons located in the segments C1 to C2 and, to a lesser degree, in C3 to C4. This pattern of supply was consistent with our labelling experiments showing extensive cervical projections of trigeminal afferents. Excitatory inputs were mediated, although not exclusively, through AMPA/kainate and NMDA receptors, whereas inhibitory inputs through both GABA and glycine receptors. In conclusion, the trigeminocervical lamina I neurons receive a complex pattern of long-range monosynaptic and polysynaptic inputs from a variety of the trigeminal nociceptive afferents.

Visually guided recordings from a novel brainstem–spinal cord preparation revealed 4 types of input from thin trigeminal afferents to the trigeminocervical lamina I neurons.

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

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

eMTA-DE Neuroscience Research Group, 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.: 00351-220408837. E-mail address: (B.V. Safronov).

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

© 2019 International Association for the Study of Pain
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