Initiation of locomotion in lampreys

• Published in: Brain Research Reviews 2008-01, Vol.57 (1), p.172-182
• Main Authors: Dubuc, Réjean, Brocard, Frédéric, Antri, Myriam, Fénelon, Karine, Gariépy, Jean-François, Smetana, Roy, Ménard, Ariane, Le Ray, Didier, Viana Di Prisco, Gonzalo, Pearlstein, Édouard, Sirota, Mikhail G, Derjean, Dominique, St-Pierre, Melissa, Zielinski, Barbara, Auclair, François, Veilleux, Danielle
• Format: Article
• Language: English
• Subjects: Acetylcholine; Animals; Brackish; Brain; Brain - anatomy & histology; Brain - physiology; Brainstem; Freshwater; Glutamate; Goal-oriented locomotion; Lampreys; Lampreys - physiology; Life Sciences; Locomotion; Locomotion - physiology; Marine; Mesencephalic locomotor region; Nervous System Physiological Phenomena; Neural Pathways; Neural Pathways - cytology; Neural Pathways - physiology; Neurology; Neurons; Neurons - physiology; Petromyzontidae; Reticulospinal; Sensation; Sensation - physiology; Sensorimotor integration
• ISSN: 0165-0173; 1872-6321
• DOI: 10.1016/j.brainresrev.2007.07.016

Abstract The spinal circuitry underlying the generation of basic locomotor synergies has been described in substantial detail in lampreys and the cellular mechanisms have been identified. The initiation of locomotion, on the other hand, relies on supraspinal networks and the cellular mechanisms involved are only beginning to be understood. This review examines some of the findings relative to the neural mechanisms involved in the initiation of locomotion of lampreys. Locomotion can be elicited by sensory stimulation or by internal cues associated with fundamental needs of the animal such as food seeking, exploration, and mating. We have described mechanisms by which escape swimming is elicited in lampreys in response to mechanical skin stimulation. A rather simple neural connectivity is involved, including sensory and relay neurons, as well as the brainstem rhombencephalic reticulospinal cells, which act as command neurons. We have shown that reticulospinal cells have intrinsic membrane properties that allow them to transform a short duration sensory input into a long-lasting excitatory command that activates the spinal locomotor networks. These mechanisms constitute an important feature for the activation of escape swimming. Other sensory inputs can also elicit locomotion in lampreys. For instance, we have recently shown that olfactory signals evoke sustained depolarizations in reticulospinal neurons and chemical activation of the olfactory bulbs with local injections of glutamate induces fictive locomotion. The mechanisms by which internal cues initiate locomotion are less understood. Our research has focused on one particular locomotor center in the brainstem, the mesencephalic locomotor region (MLR). The MLR is believed to channel inputs from many brain regions to generate goal-directed locomotion. It activates reticulospinal cells to elicit locomotor output in a graded fashion contrary to escape locomotor bouts, which are all-or-none. MLR inputs to reticulospinal cells use both glutamatergic and cholinergic transmission; nicotinic receptors on reticulospinal cells are involved. MLR excitatory inputs to reticulospinal cells in the middle (MRRN) are larger than those in the posterior rhombencephalic reticular nucleus (PRRN). Moreover at low stimulation strength, reticulospinal cells in the MRRN are activated first, whereas those in the PRRN require stronger stimulation strengths. The output from the MLR on one side activates reticulospinal neurons on bo