Deafferenting injuries often cause transient or permanent physiological alterations within the central projection field of affected primary afferent fibers. Aberrant sensory perceptions, dysesthesias, and hyperalgesias represent the clinical sequelae of such injuries; however, the results of experimental deafferentations have been subject to a variety of interpretations (Rodin and Kruger, 1984b). Neurochemical studies show an increased sensitivity of partially deafferented neurons to substance P (SP). Our previous studies (Hoffmann et al., 1991) documented, primarily at the light-microscopic level, a moderate transient loss of SP-immunoreactive (SPIR) boutons in the trigeminal subnucleus caudalis (Vc)--a loss that seemed to preferentially affect the slightly larger, possibly complex boutons with multiple contacts. However, despite the elimination of the trigeminal input, the larger boutons reappeared. In the present study, therefore, we examined Vc using electron-microscopic immunocytochemistry, in order to document these changes over time and to clarify the structure and relationships of this population of boutons. SPIR boutons occurred in lamina I and II degrees of the substantia gelatinosa of Vc, ranged in size from 1 to 5 microns in diameter, and displayed mixed populations of clear and dense-core vesicles. Most formed single or multiple axodendritic junctions, but a significant number engaged in axoaxonic contacts with both SPIR-labeled and unlabeled terminals. A small number appeared to be the central element of a typical glomerulus, particularly in lamina II degrees. Three to seven days following an ipsilateral retrogasserian rhizotomy, synaptic degeneration was evident in the substantia gelatinosa and often involved glomerular terminals. However, most of these were SPIR-negative and occurred primarily in lamina II degrees. Those SPIR boutons that displayed degenerative features often made single or multiple axodendritic contacts, and in some instances were scalloped. By 30 days, most remaining SPIR boutons were small, with a lower incidence of contacts; however, some of these were axoaxonic. In addition, many SPIR terminals were only very lightly stained--a feature not encountered to such an extent in the contralateral Vc. At 45 days, complex SPIR boutons were again evident in the field, and some showed densely packed vesicles. An increased incidence of clusters of two to four SPIR axoaxonic contacts was also observed. Finally, almost all SPIR boutons encountered at this stage were intensely stained. It is suggested that these alterations represent a compensatory neuroplastic response on the part of overlapping cervical and cranial primary afferents to the partial deafferentation resulting from the interruption of the trigeminal root.(ABSTRACT TRUNCATED AT 400 WORDS)