Cell‐type‐specific excitatory and inhibitory circuits involving primary afferents in the substantia gelatinosa of the rat spinal dorsal horn in vitro

Abstract

The substantia gelatinosa (SG) of the spinal dorsal horn shows significant morphological heterogeneity and receives primary afferent input predominantly from Aδ-and C-fibres. Despite numerous anatomical and physiological studies, correlation between morphology and functional connectivity, particularly in terms of inhibitory inputs, remains elusive. To compare excitatory and inhibitory synaptic inputs on individual SG neurones with morphology, we performed whole-cell recordings with Neurobiotin-filled-pipettes in horizontal slices from adult rat spinal cord with attached dorsal roots. Based on dendritic arborization patterns, four major cell types were confirmed: islet, central, radial and vertical cells. Dorsal root stimulation revealed that each class was associated with characteristic synaptic inputs. Islet and central cells had monosynaptic excitatory inputs exclusively from C-afferents. Islet cells received primary-afferent-evoked inhibitory inputs only from Aδ-fibres, while those of central cells were mediated by both Aδ-and C-fibres. In contrast, radial and vertical cells had monosynaptic excitatory inputs from both Aδ-and C-fibres and inhibitory inputs mediated by both fibre types. We further characterized the neurochemical nature of these inhibitory synaptic inputs. The majority of islet, central and vertical cells exhibited GABAergic inhibitory inputs, while almost all radial cells also possessed glycinergic inputs. The present study demonstrates that SG neurones have distinct patterns of excitatory and inhibitory inputs that are related to their morphology. The neurotransmitters responsible for inhibitory inputs to individual SG neurones are also characteristic for different morphological classes. These results make it possible to identify primary afferent circuits associated with particular types of SG neurone.

Heterosynaptic Long-Term Potentiation at GABAergic Synapses of Spinal Lamina I Neurons

“…Previous work indicates that most neurons located in lamina I of the spinal cord, being either excitatory or inhibitory, receive monosynaptic input from either A␦-fibers and/or C-fibers (Yoshimura and Jessell, 1990;Dahlhaus et al, 2005;Yasaka et al, 2007;Pinto et al, 2010), and many also express group I mGluRs (Alvarez et al, 2000). In the present study, we recorded from unidentified lamina I neurons and showed that LTP GABA could Figure 7.…”

A feed-forward spinal cord glycinergic neural circuit gates mechanical allodynia

“…This suggests that many inhibitory interneurons corelease GABA and glycine, whereas others release only GABA. However, electrophysiological studies have identified synapses in this region that are purely Gly (3,54,55). Although these may involve axons that originate from Gly neurons located outside laminae I-III, in many cases the lack of a GABAergic component prob ably results from the absence of GABAA receptors at these synapses (3).…”

The Inhibitory Neuronal Circuit of Spinal Cord in Neuropathic Pain

“…Central cells receive excitatory inputs from C-afferents and primary-afferentevoked inhibitory inputs mediated by both Aδ-and C-fibres. The excitatory inputs to radial cells were mediated by both Aδ-and C-fibres (17). In addition, the lamina II central, and the radial cells, receive an intralaminar-derived inhibitory input from islet cells.…”

“…Islet cells and central cells were located in lamina Ili, IIo and near the border of laminae Ili and IIo. Their dendritic trees spread in the rostrocaudal direction (17). Somata of vertical neurons located in lamina IIo and pass ventrally through laminae II -IV.…”

“…Radial cells extend in several directions in lamina II. All islet cells are inhibitory neurons with immunocytochemical features of GABAergic cells (17). Central cells include both excitatory and inhibitory neurons.…”