Trigeminal and spinal dorsal horn (dis)continuity and avian evolution

The organization of the dorsal horn in the avian spinal cord differs in different species. For instance, in pigeons and doves, cranes, cuckoos, songbirds, ratites and tinamous, the dorsal horn is organized in laminar fashion, such that laminae II and III are sandwiched between lamina I dorsally and lamina IV ventrally, as they are in mammals and other nonavian amniotes. In most other avian species, including chickens, however, the organization of the dorsal horn is not strictly laminar, in that the structures homologous to laminae II and III lie side by side rather than in dorsoventral order. Because spinal and trigeminal dorsal horns are generally thought to be continuous, the question arises as to the organization of the trigeminal dorsal horn in these species. We examined this question in chickens, first by defining II and III of trigeminal and spinal dorsal horns using calcium-binding protein immunohistochemistry, and second by determining the caudal extent of the projections of the three branches of the trigeminal nerve using injections of cholera toxin B chain. It was found (1) that the trigeminal dorsal horn and the spinal dorsal horn of the first 2 cervical segments are organized in laminar fashion, but further caudally, II and III in the spinal dorsal horn gradually come to be arranged side by side and (2) that the descending trigeminal tract terminates no further caudal than the 3rd spinal segment. Therefore, unlike spinal nerves, trigeminal nerve branches do not project to II and III, once these cease to be organized in laminar fashion. These findings imply some kind or organizational discontinuity of trigeminal and spinal dorsal horns in the chicken and perhaps in other species with a side-by-side arrangement of II and III. It has also been suggested that the condition in which the spinal dorsal horn structures homologous to laminae II and II lie side by side may define a novel clade of birds. This suggestion was reexamined within the context of a modern phylogenetic framework based on 32 kb of nuclear DNA, and using a parsimony reconstruction of dorsal horn character states. The original suggestion of a novel clade was not supported. Instead, it appears that the side-by-side condition evolved very early in the radiation of Aves and that independent reversion to a laminar dorsal horn condition has evolved at least 4-5 times.