An EM analysis of the synaptic connections of horseradish peroxidase‐filled stalked cells and islet cells in the substantia gelatinosa of adult cat spinal cord

Abstract

Two major interneurons of the outer part of Rexed's layer I1 (IIa) were impaled with microelectrodes, had their primary inputs characterized, and were subsequently filled with horseradish peroxidase. Their fine structural characteristics and synaptic connections were then analyzed electron microscopically. Two islet cells, whose rostrocaudally oriented dendrites were largely confined within layer IIa, received primary input from small myelinated axons. A stalked cell, whose cell body was situated on 1/11 border had a cone-shaped dendritic arbor which traversed layer IIa as well as the inner part of Rexed's layer I1 (IIb) and rostrocaudal dendritic branches which ran for part of their course along the UIIa border. It received primary input from small myelinated as well as from unmyelinated axons. Both cell types received asymmetrical axodendritic synapses from primary endings in layer IIa and IIb glomeruli and widely separated symmetrical axodendritic synapses from small nonprimary endings outside of glomerli.The presence of aggregates of synaptic vesicles in the dendrites of the layer IIa islet cells but not in the stalked cell dendrites constitutes the major fine structural difference between these interneurons. Islet cell dendrites form symmetrical synapses on several different kinds of neural processes. They usually send either a single type 2 spine (spines which contain synaptic vesicles) or dendritic shaft into layer IIa and IIb glomeruli, where they form dendrodendritic synapses on adjacent type 1 spines (spines without synaptic vesicles) and on other small dendritic shafts. Some islet cell type 2 spines also form dendroaxonic synapses on the primary endings.Outside of the glomeruli, islet cell dendrites also form dendrodendritic synapses on type 1 spines and different sized dendritic shafts. They often approach other dendritic shafts forming small bundles of dendrites in which they are reciprocally linked by dendrodendritic synapses to other synaptic vesicle-containing dendrites. At bead-like enlargements of their dendritic shafts and along some of their fine caliber dendritic shafts, the islet cells form dendroaxonic synapses on the shafts of unmyelinated axons. The unmyelinated axon of the islet cell forms symmetrical synapses on layer I1 dendritic shafts and spines outside of glomeruli. The role of the layer IIa islet cell as an inhibitory interneuron is discussed.

Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex

“…In addition to dendritic trees that are most extensive rostrocaudally, substantia gelatinosa neurons often have unusually complex dendritic branching and dendritic spines (Scheibel and Scheibel, 1969;Light et al, 1979;Gobel et al, 1980;Rethelyi et al, 1989;Ramon y Cajal, 1995;Grudt and Perl, 2002), similar to a subset of flexion cells found in the dorsomedial dorsal horn in this study (Fig. 6 B).…”

“…The rostrocaudally extensive but mediolaterally and dorsoventrally compact dendritic trees of most flexion cells seen here are similar to those of cutaneously activated local axon cells in laminas III-V of the hamster dorsal horn (Schneider, 1992), cat glutamatergic group II-activated dorsal horn interneurons (Bannatyne et al, 2006), and many cat and rodent laminas II-IV cells generally (Scheibel and Scheibel, 1969;Rethelyi et al, 1989), including cells responsive to innocuous or noxious mechanical stimuli (Light et al, 1979;Gobel et al, 1980). In addition to dendritic trees that are most extensive rostrocaudally, substantia gelatinosa neurons often have unusually complex dendritic branching and dendritic spines (Scheibel and Scheibel, 1969;Light et al, 1979;Gobel et al, 1980;Rethelyi et al, 1989;Ramon y Cajal, 1995;Grudt and Perl, 2002), similar to a subset of flexion cells found in the dorsomedial dorsal horn in this study (Fig.…”

Modular Organization of Excitatory Circuits between Neurons of the Spinal Superficial Dorsal Horn (Laminae I and II)

“…The CV of the dorsal-root input to the presynaptic lamina II o neurons averaged 1.2 Ϯ 0.1 m/s, also equivalent to DR A␦ CVs for the postsynaptic vertical cells in the transient-to-vertical neuron connection. Projection of a vertical type of lamina II neuron to a lamina I neuron has been suggested before on circumstantial morphological and physiological grounds (Gobel, 1978;Bennett et al, 1980;Gobel et al, 1980;Ramon y Cajal, 1999). The present evidence represents the first proven demonstration of functional connections between these cell types.…”

Heat-evoked responses of dorsal horn nociceptive neurons in the monkey.

“…Results reported by Dubner and his group (PRICE et al, , 1979BENNETT et al, 1980;GoBEL et al, 1980) are somewhat different:…”