Functional properties and axon terminations of interneurons in laminae III-V of the mammalian spinal dorsal horn in vitro.

1. The functional organization of interneurons in spinal laminae III-V was studied in an isolated preparation of hamster dorsal horn with sensory innervation from an excised skin patch. Morphological details of 40 neurons were visualized by intracellular injection of horseradish peroxidase. Active and passive membrane properties, synaptic responses to cutaneous nerve volleys, and responses to innocuous mechanical stimuli were determined for 25 cells with identified axons. 2. Neurons were classified into two types: 1) cells with local axons, branching in proximity to the cell soma and dendrites, that produced numerous synaptic boutons (740 +/- 504/axon; mean +/- SD), often arranged in clusters and 2) neurons with deep axons that usually bifurcated into rostral and caudal daughter branches up to 2.5 mm long, giving off collaterals ventral to the cell body and dendrites and forming significantly fewer boutons (155 +/- 140/axon) than local axon cells. A majority of boutons of local axon and deep axon cells, 89 and 83%, respectively, were of the en passant type. 3. Dendritic trees of local axon cells were relatively compact dorsoventrally (119 +/- 42 microns) and mediolaterally (128 +/- 45 microns), but were elongated rostrocaudally (404 +/- 121 microns). In comparison, dendritic trees of deep axon cells radiated significantly farther dorsoventrally (218 +/- 88 microns) and mediolaterally (180 +/- 34 microns), but exhibited comparable rostrocaudal spread (413 +/- 128 microns). There was no correlation between dorsoventral and mediolateral dendritic spread and mediolateral soma location for either cell type. However, for medially situated deep axon cells the rostrocaudal dendritic spread was up to 180% greater than for those located laterally. For nearly one-half of all cells (49%; 17/35) dendritic processes extended dorsally into lamina II. 4. Local axon cells had resting membrane potentials that were more negative than deep axon cells (-59.5 +/- 6.1 and -53.6 +/- 4.7 mV, respectively), but the amplitude and duration of action potentials generated by the two types were similar. Neuronal input resistance (RN) and membrane time constant (tau m) varied widely from cell to cell, but were not significantly different for local axon (77.4 +/- 46.8 M omega, 13.4 +/- 9.5 ms) and deep axon cells (46.5 +/- 19.2 M omega, 6.6 +/- 3.0 ms). 5. Volleys in myelinated afferent fibers activated fast rising excitatory postsynaptic potentials (EPSPs) that exhibited later, more slowly rising potentials with multiple components in a majority of deep axon (89%) and local axon (72%) neurons.(ABSTRACT TRUNCATED AT 400 WORDS)