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

Abstract

SUMMARY Dopamine (DA) activates fictive crawling behavior in the medicinal leech. To identify the cellular mechanisms underlying this activation at the level of crawl-specific motoneuronal bursting, we targeted potential cAMP-dependent events that are often activated through DA 1 -like receptor signaling pathways. We found that isolated ganglia produced crawl-like motoneuron bursting after bath application of phosphodiesterase inhibitors (PDIs) that upregulated cAMP. This bursting persisted in salines in which calcium ions were replaced with equimolar cobalt or nickel, but was blocked by riluzole, an inhibitor of a persistent sodium current. PDI-induced bursting contained a number of patterned elements that were statistically similar to those observed during DA-induced fictive crawling, except that one motoneuron (CV) exhibited bursting during the contraction rather than the elongation phase of crawling. Although DA and the PDIs produced similar bursting profiles, intracellular recordings from motoneurons revealed differences in altered membrane properties. For example, DA lowered motoneuron excitability whereas the PDIs increased resting discharge rates. We suggest that PDIs (and DA) activate a sodium-influx-dependent timing mechanism capable of setting the crawl rhythm and that multiple DA receptor subtypes are involved in shaping and modulating the phase relationships and membrane properties of cell-specific members of the crawl network to generate crawling.

The Integrative Role of the Sigh in Psychology, Physiology, Pathology, and Neurobiology

“…6B). This principle has been well documented in a variety of invertebrate (Crisp et al, 2012; Dickinson and Nagy, 1983; Khorkova and Golowasch, 2007; Ramirez and Pearson, 1991a,b; Zhao and Golowasch, 2012) and other mammalian networks (Kolaj et al, 2007; Mrejeru et al, 2011; Tsuruyama et al, 2013). Within the respiratory network, multiple neuromodulators, such as serotonin, norepinephrine, acetylcholine, or substance P,can alter the distribution of these activities (Doi and Ramirez, 2008; Ramirez et al, 2012; Fig.…”

Dopamine: a parallel pathway for the modulation of spinal locomotor networks

“…These actions are a result of a complex modulation of intrinsic cellular properties and synaptic connectivity (for review see Harris-Warrick et al, 1998). Remarkably, in some species dopamine demonstrates the ability to reconfigure circuits or networks to generate completely different motor behaviors (Puhl and Mesce, 2008; Crisp et al, 2012; Puhl et al, 2012). More recent studies have highlighted the ability of dopamine to shape a motor network during development, producing a change in motor behaviors from immature to more mature adult-like behaviors (Lambert et al, 2012).…”

“…Specifically, dopamine acts as a command signal to elicit crawling along with suppression of swimming (Puhl and Mesce, 2008; Crisp et al, 2012; Puhl et al, 2012), and is an excellent example of the ability of dopamine to bias locomotor behavior (Crisp and Mesce, 2004). Dopamine has a similar effect in nematodes (e.g., Caenorhabditis elegans) where it also acts to bias locomotor activity to a crawl pattern of activity over swimming (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.…”