Gap junction protein in weakly electric fish (gymnotide): Immunohistochemical localization with emphasis on structures of the electrosensory system

Abstract

Electrotonic transmission via gap junctions appears to be essential for both the relay and integration of information in nuclear groups involved in the electrolocation and electrocommunication systems of weakly electric fish. An affinity-purified antibody against the 27 kD gap-junctional polypeptide (GJP) from rat liver was used to determine immunohistochemically the distribution of GJP-immunoreactivity (GJP-IR) in electrosensory structures and some other brain regions of the gymnotiform fish, Apteronotus leptorhynchus. At the ultrastructural level, immunolabelling with this antibody was localized, in part, to neuronal and glial gap junctions where it was assumed to recognize a junctional polypeptide. By light microscopy, the vast majority of immunoreactive elements appeared either as fine puncta or as varicosities along fibers that exhibited immunostained intervaricose segments. Diffuse immunoreactivity within cell bodies was rare, being most evident in giant relay neurons and presumptive glial cells within the pacemaker nucleus and in neurons within the posterior raphe nucleus. The distribution of punctate and fibrous GJP-IR was remarkably heterogeneous with respect to density; large areas of the forebrain and most major fiber tracts were nearly devoid of immunoreactivity, whereas concentrations of puncta delineating patches within the inferior lobe of the hypothalamus and the vagal sensory nucleus were so dense as to appear as uniform deposition of immunoperoxidase reaction product at low magnification. Some structures known to be associated with the electrosensory system, including the nucleus electrosensorius and nucleus praeeminentialis, were among the brain regions containing the highest concentrations of immunoreactivity. At the cellular level, expected patterns of GJP-IR were observed in the pacemaker nucleus, torus semicircularis, and electrosensory lateral line lobe. In each of these structures punctate immunoreactivity was seen in apposition to cell bodies or dendrites of neurons known to receive gap junction contacts. In addition, the dendrites of neurons within the prepacemaker nucleus were laden with a striking array of puncta, suggesting that interactions via gap junctions may be a significant feature of these neurons. These immunohistochemical results are consistent with previous electrophysiological and ultrastructural observations pointing to the importance of electrotonic communication in the electrosensory system of weakly electric fish, and suggest that gap junctions may also contribute to neural transmission in central nervous system related to other functions in these teleosts.(ABSTRACT TRUNCATED AT 400 WORDS)