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J Physiol Volume 581, Number 1, 241-254, May 15, 2007 DOI: 10.1113/jphysiol.2006.126912
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NEUROSCIENCE

Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat

Sónia F. A. Santos1,2, Sandra Rebelo2, Victor A. Derkach3 and Boris V. Safronov1,2

1 Instituto de Biologia Molecular e Celular – IBMC, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal
2 Laboratório de Biologia Celular e Molecular, Faculdade de Medicina, Universidade do Porto, Alameda Professor Hernâni Monteiro, 4200-319 Porto, Portugal
3 Vollum Institute, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239, USA

Substantia gelatinosa (SG, lamina II) is a spinal cord region where most unmyelinated primary afferents terminate and the central nociceptive processing begins. It is formed by several distinct groups of interneurons whose functional properties and synaptic connections are poorly understood, in part, because recordings from synaptically coupled pairs of SG neurons are quite challenging due to a very low probability of finding connected cells. Here, we describe an efficient method for identifying synaptically coupled interneurons in rat spinal cord slices and characterizing their excitatory or inhibitory function. Using tight-seal whole-cell recordings and a cell-attached stimulation technique, we routinely tested about 1500 SG interneurons, classifying 102 of them as monosynaptically connected to neurons in lamina I–III. Surprisingly, the vast majority of SG interneurons (n = 87) were excitatory and glutamatergic, while only 15 neurons were inhibitory. According to their intrinsic firing properties, these 102 SG neurons were also classified as tonic (n = 49), adapting (n = 17) or delayed-firing neurons (n = 36). All but two tonic neurons and all adapting neurons were excitatory interneurons. Of 36 delayed-firing neurons, 23 were excitatory and 13 were inhibitory. We conclude that sensory integration in the intrinsic SG neuronal network is dominated by excitatory interneurons. Such organization of neuronal circuitries in the spinal SG can be important for nociceptive encoding.

(Received 21 December 2006; accepted after revision 28 February 2007; first published online 1 March 2007)
Corresponding authors B. V. Safronov: Instituto de Biologia Molecular e Celular-IBMC, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal.  Email: safronov{at}ibmc.up.pt

V. A. Derkach: Vollum Institute, Oregon Health & Science University, 3181 SW Sam Jackson Park Rd, Portland, OR 97239, USA.  Email: derkachv{at}ohsu.edu




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