**The title, authors, and abstract for this completion report are provided below. For a copy of the completion report, please contact the GLFC via e-mail or via telephone at 734-662-3209**
The neural mechanisms underlying pheromone activated movement in lampreys
Barbara Zielinski1 and Rejéan Dubuc2
1Dept. of Biological Sciences,
Universityof Windsor, Windsor, Ontario N9B 3P4
2 Dept. Kinesiology, Université du Québec à Montréal, PO Box 8888, Succ. Centre-ville, Montréal, Quebec H3P 3P8
This two-year study was conducted to gain understanding of the neurobiology behind pheromone-activated movement in the sea lamprey (Petromyzon marinus). Neuronal tract-tracing and electrophysiological recordings point to the existence of a specific neural pathway dedicated to transforming olfactory sensory input into locomotor output in the sea lamprey – the first time that this pathway has been identified in any vertebrate. Supporting data have been incorporated into three manuscripts. Manuscript 1 (Laframboise et al., 2007) has been published, Manuscript 2 (Ren et al.) is in the final stages of preparation for submission and Manuscript 3 (Derjean et al.) requires additional control experiments before submission to a high-impact journal. We aim to publish Derjean et al. in the journal Science because this study is the first demonstration of neural connectivity between the olfactory system and locomotor control centers in the brain in any vertebrate species. Manuscript 1 demonstrated that olfactory epithelium located in the caudo-ventral region of the peripheral olfactory organ, which responds to odorant (including pheromone) stimulation, contains intermixed polymorphic olfactory sensory neurons. These cell types resemble those previously observed in teleost fish, which express specific receptor proteins. This study suggests that lamprey olfactory sensory neurons may have specific morphological subtypes that respond to pheromones. Manuscript 2 pertains to the accessory olfactory organ, a duct-like invagination, also located in the caudoventral region of the peripheral olfactory organ. We have shown that this structure contains putative olfactory sensory neurons that project into a spatially defined medial region of the olfactory bulb. These cells are significant for pheromone (odorant) – locomotion neurobiology because they project to the neural pathway that stimulates movement in response to olfactory inputs, discovered by Derjean et al. in Manuscript 3. We will apply the formatting requirements for Science to Manuscript 3 once results from additional control experiments have been incorporated. Derjean et al. have demonstrated that the medial territory of the olfactory bulb (which receives the axons from accessory olfactory organ) drives a neural circuit that links the peripheral olfactory organ to locomotor output. This manuscript shows that odorant (including pheromone) application onto the olfactory epithelium stimulated responses from the olfactory bulb, as well as large sustained depolarizations from reticulospinal neurons, the command neurons that directly activate spinal networks for locomotion. Stimulation of the medial region of the olfactory bulb elicited large excitatory responses in the reticulospinal cells, whereas stimulating lateral bulbar regions failed to activate these cells. Locomotion was also elicited following application of the excitatory neurotransmitter, glutamate, onto the olfactory bulb. Anterograde and retrograde tract tracing experiments demonstrated two neural projection patterns extending from the olfactory bulb. Neurons located in the medial region of the olfactory bulb projected directly to the posterior tuberculum, a diencephalic region with neuronal connections to locomotor centres. A second neural projection, largely from non-medial bulbar territories, projected to the lateral pallium, a forebrain integrative center. These results suggest that a specific neural pathway links olfactory sensory input to locomotion, and a second pathway that could be involved in processing odour identification and perception. The Derjean study is especially significant – it is the first to show the neural pathway and some of the mechanisms underlying the transformation of an olfactory input into a locomotor output in a vertebrate species. The hard-wiring of this pathway may be present from the transformer to the reproductive adult stages, however how this pathway becomes activated during pheromone stimulated movement at the appropriate developmental stage, remains unknown.