Dopamine Activates the Motor Pattern for Crawling in the Medicinal Leech

Abstract

Locomotion in segmented animals is thought to be based on the coupling of "unit burst generators," but the biological nature of the unit burst generator has been revealed in only a few animal systems. We determined that dopamine (DA), a universal modulator of motor activity, is sufficient to activate fictive crawling in the medicinal leech, and can exert its actions within the smallest division of the animal's CNS, the segmental ganglion. In the entire isolated nerve cord or in the single ganglion, DA induced slow antiphasic bursting (ϳ15 s period) of motoneurons known to participate in the two-step elongation-contraction cycle underlying crawling behavior. During each cycle, the dorsal (DE-3) and ventral (VE-4) longitudinal excitor motoneurons fired ϳ180°out of phase from the ventrolateral circular excitor motoneuron (CV), which marks the elongation phase. In many isolated whole nerve cords, DE-3 bursting progressed in an anterior to posterior direction with intersegmental phase delays appropriate for crawling. In the single ganglion, the dorsal (DI-1) and ventral (VI-2) inhibitory longitudinal motoneurons fired out of phase with each DE-3 burst, further confirming that the crawl unit burst generator exists in the single ganglion. All isolated ganglia of the CNS were competent to produce DA-induced robust fictive crawling, which typically lasted uninterrupted for 5-15 min. A quantitative analysis indicated that DA-induced crawling was not significantly different from electrically evoked or spontaneous crawling. We conclude that DA is sufficient to activate the full crawl motor program and that the kernel for crawling resides within each segmental ganglion.

Mechanisms contributing to the dopamine induction of crawl-like bursting in leech motoneurons

“…Parameters and methods used to measure crawl-related burst cycle periods and durations were those of Puhl and Mesce (Puhl and Mesce, 2008;Puhl and Mesce, 2010) and typically involved bursts that had clearly discernable onsets. A minimum of six to 10 consecutive bursts were analyzed for each preparation and means were compared across the number (N) of preparations tested.…”

“…Although DA has been convincingly demonstrated to activate fictive crawling, even in a single ganglion (Puhl and Mesce, 2008), the subcellular and biochemical mechanisms underlying such activation have yet to be explored. To begin to identify these mechanisms, we sought to determine whether crawling-related activity was dependent on cAMP second-messenger signaling.…”

“…In the medicinal leech, for example, DA has been shown to activate the central pattern generator (CPG) underlying crawling behavior (Puhl and Mesce, 2008;Puhl and Mesce, 2010). DA also serves an important function in the selection of competing or incompatible behaviors, exemplified by its suppression of swimming activity in the leech (Crisp and Mesce, 2004).…”

Multiplexed modulation of behavioral choice

“…Dopamine, as well as serotonin, is known to play a role in the decision to swim or crawl. In the leech, dopamine has been found to bias behavioral choice toward crawling (Crisp and Mesce, 2004;Puhl and Mesce, 2008), whereas serotonin makes swimming more likely (Friesen and Kristan, 2007). Caenorhabditis elegans also uses dopamine and serotonin to set the balance between these two locomotory behaviors (Vidal-Gadea et al, 2011).…”

Intracellular Recording, Sensory Field Mapping, and Culturing Identified Neurons in the Leech, <i>Hirudo medicinalis</i>

“…Neuromodulation, particularly through biogenic amine pathways, has also been a successful research direction in the leech. By adding dopamine and other pharmacological agents to the nervous system through the saline solution, it has been shown that dopamine modulates neural networks involved in decision-making 23 and motor patterns for crawling behavior 24,25 . This experimental approach is a simple (and inexpensive) way to incorporate modulation into the teaching laboratory, and adjusting the ionic makeup of the saline solution is an effective way to teach the Nernst and Goldman-Hodgkin-Katz equations.…”