Primary olfactory fibres project to the ventral telencephalon and preoptic region in trout (Salmo trutta): A developmental immunocytochemical study

Abstract

We studied the development of the primary olfactory system of a teleost, the brown trout, with the aims of clarifying whether the caudal projection pertains to the olfactory or to the terminal nerve system, of identifying the brain regions receiving this projection, and of investigating its possible functional significance. As olfactory markers (OMs) we used two polyclonal antibodies (to substance P and to alpha-melanocyte-stimulating hormone) that were found to label the olfactory projection strongly after preadsortion of the antibody with the corresponding antigen (OMs), and as a terminal nerve marker we used an antiserum to FMRF-amide peptide. OM labelling was observed in both perikarya and axons of olfactory neurons. In adults, olfactory neurons projected not only to olfactory glomeruli in the olfactory bulb but also, as has been reported previously, to more caudal targets in the forebrain through the medial olfactory tract. Our results show that these targets include the ventral and commissural nuclei of the area ventralis telencephali, the periventricular preoptic region, and the organum vasculosum laminae terminalis. Glomeruli were not observed before hatching, and the extrabulbar olfactory projections appear late in development. Extensive periventricular preoptic olfactory plexuses and olfactory innervation of the organum vasculosum laminae terminalis did not appear until adulthood. The cells of the ganglion nervus terminalis, which form ganglionic groups along the olfactory nerves, were not stained with these olfactory markers at any developmental stage studied, nor was the medial olfactory tract FMRP-amide peptide immunoreactive. Our results thus confirm the existence of primary olfactory projections to extrabulbar targets in trout. The target regions identified in this study are implicated in sexual behaviour: We discuss the related possibility that, in teleosts, these extrabulbar olfactory projections (rather than projections of the terminal nerve, as is widely held) are the primary mediators of neuroendocrine response to pheromones.

Development of immunoreactivity to neuropeptide Y in the brain of brown trout (Salmo trutta fario)

“…The terminal ganglion also contains gonadotropin-releasing hormone and FMRF-amide peptide (Kah et al, 1986;Grober et al, 1987;Ekström et al, 1988;Ö stholm et al, 1990;Rama Krishna et al, 1992;Chiba et al, 1996;Chiba, 1997). FMRF-amide and NPY probably are colocalized in trout, because all terminal ganglion cells in developing fish appear to contain these two peptides (Becerra et al, 1994;current results).…”

“…The NPY-ir cells of the ventrolateral telencephalic area and the hypothalamus appear early during development, but they become considerably more abundant at later stages. The relatively early appearance of NPY-ir cells in Vl contrasts with the late maturation of the olfactory bulbs (Manso et al, 1993;Becerra et al, 1994). The great increase in the numbers of NPY-ir cells in this telencephalic area observed in alevins and fry may be related to maturation of the olfactory system and of circuits in the dorsal telencephalon coinciding with exhaustion of egg-yolk stores.…”

Food Web Structure Shapes the Morphology of Teleost Fish Brains

“…The olfactory bulbs are paired structures, located at the rostral end of the brain, that receive chemosensory input from olfactory receptor neurons located in the olfactory rosettes [Hara, 1992;Laberge and Hara, 2001]. Projection neurons of the olfactory bulbs (the mitral cells) then send olfactory information to the telencephalon [Becerra et al, 1994]. The telencephalon is the primary site for higher-order integrative brain functions [Davis et al, 1981;Davis and Kassel, 1983].…”

Development of the Terminal Nerve System in the Shark <b><i>Scyliorhinus canicula</i></b>

“…It is interesting to note that in elasmobranchs, terminal nerve ganglion cells remain outside the forebrain, forming peripheral ganglia Wu et al, 1992;Forlano et al, 2000;Yáñez et al, 2011]. This is in contrast to bony fishes in which during development clusters of terminal nerve ganglion cells associated with the ON eventually migrate into the OB and basal telencephalon [Halpern-Sebold and Schreibman, 1983;Münz and Claas, 1987;Becerra et al, 1994;Parhar et al, 1995;Chiba et al, 1996;Prego et al, 2002;Whitlock, 2004;Biju et al, 2005].…”