Bursts of Information: Coordinating Interneurons Encode Multiple Parameters of a Periodic Motor Pattern

Abstract

The limbs on different segments of the crayfish abdomen that drive forward swimming are directly controlled by modular pattern-generating circuits. These circuits are linked together by axons of identified coordinating interneurons. We described the distributions of these neurons in each abdominal ganglion and monitored their firing during expression of the swimming motor pattern. We analyzed the timing, the numbers of spikes, and the duration of each burst of spikes in these coordinating neurons. To see what information these neurons encoded, we correlated these parameters with the timing, durations, and strengths of bursts of spikes in motor axons from the same modules. During the power-stroke phase of each output cycle, the anterior-projecting neurons fired bursts of spikes that encoded information about the start-time, duration, and strength of each burst of spikes in power-stroke motor neurons from the same module. When the period and intensity of the motor output fluctuated, the bursts of spikes in these neurons tracked these fluctuations accurately. Each additional spike in these neurons signified an increase in the strength of the power-stroke burst. The posterior-projecting neurons that fired during the return-stroke phase encoded similar information about the return-stroke motor neurons. Although homologous neurons from different ganglia were qualitatively similar, neurons from posterior ganglia fired significantly more spikes per burst than those from more anterior ganglia, a segmental gradient that correlates with the normal posterior-to-anterior phase progression of limb movements. We propose that this gradient and a similar gradient in the durations of bursts in power-stroke motor neurons might reflect a hitherto-undetected difference in the excitation or intrinsic excitability of swimmeret modules in different segments.

A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity

“…Moreover, it is clear in the gastric mill network that "descending modulatory inputs" are important elements in rhythm generation (Hooper and DiCaprio 2004;Marder and Bucher 2001;Nusbaum and Beenhakker 2002). Clear separation between local interneurons concerned with rhythm generation and local motor patterning (Paul and Mulloney 1985) and interneurons involved in intersegmental coordination (i.e., elaborating intersegmental pattern) appears to occur in the swimmeret system of crayfish; these coordinating interneurons are not apparently premotor, however (Mulloney and Hall 2003;Mulloney et al 1998Mulloney et al , 2006. In the leech swimming central pattern generator, rhythm generation, local pattern elaboration, and intersegmental coordination are all shared by key network interneurons (Kristan et al 2005), although intersegmental coordination relies heavily on sensory feedback Friesen 2000, 2002).…”

“…For example, some pattern generators produce segmentally distributed output, such as that controlling undulatory swimming Friesen 2000, 2002;De Schutter et al 2005;Grillner et al 2005;Kristan et al 2005), so that a conceptual separation between rhythm generation as expressed in side-to side or dorsal-ventral alternation and pattern formation as expressed in intersegmental coordination seems clear, although key elements involved in intersegmental coordination appear integral to rhythm generation. The crayfish swimmeret system stands in stark contrast here with network elements clearly separated along these functional lines (Mulloney et al 1998(Mulloney et al , 2006Paul and Mulloney 1985). Clearly separating these functions in any given circuit may help us extract useful generalization for other networks controlling similar movements and again quantitative assessment of network activity is a necessary step.…”

A Central Pattern Generator Producing Alternative Outputs: Phase Relations of Leech Heart Motor Neurons With Respect to Premotor Synaptic Input

“…The stomatogastric CPGs are also not well suited to illuminate distributed CPGs that control and coordinate intersegmental motor outflow because of their local output. In the swimmeret CPG of crayfish (Mulloney and Hall 2007;Mulloney et al 2006), and especially in the leech swimming CPG (Cang and Friesen 2002;Kristan et al 2005), such quantitative descriptions of interneuron and motor neuron coordination are gradually emerging. Much progress is now being made in identifying the key neuronal elements that make up vertebrate pattern generators, and the fictive motor programs are often well described (Grillner et al 2005;Kiehn 2006), although relative coordination has not been well quantified.…”

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

“…Rhythmic bursts of motor neurone spikes are generated by chains of serially repeated pairs of CPGs, one in each hemiganglion, that are interconnected both bilaterally across the midline and across abdominal segments Wiersma and Ikeda, 1964). The local pattern-generating circuits, including nonspiking local interneurones, and the pathways for intersegmental coordination have been well characterized by the detailed studies of Mulloney and colleagues (Mulloney and Hall, 2000;Mulloney and Hall, 2003;Mulloney and Hall, 2007;Mulloney et al, 2006;Paul and Mulloney, 1985;Smarandache et al, 2009;SmarandacheWellmann et al, 2013;Smarandache-Wellmann et al, 2014; for a review, see Mulloney and Smarandache, 2010;Mulloney and Smarandache-Wellmann, 2012). There is, however, almost no evidence that the rhythmic beating activity of the swimmeret motor neurones is affected by NO.…”