Variability of Motor Neuron Spike Timing Maintains and Shapes Contractions of the Accessory Radula Closer Muscle ofAplysia

Abstract

The accessory radula closer (ARC) muscle of Aplysia has long been studied as a typical "slow" muscle, one that would be assumed to respond only to the overall, integrated spike rate of its motor neurons, B15 and B16. The precise timing of the individual spikes should not much matter. However, but real B15 and B16 spike patterns recorded in vivo show great variability that extends down to the timing of individual spikes. By replaying these real as well as artificially constructed spike patterns into ARC muscles in vitro, we examined the consequences of this spike-level variability for contraction. Replaying the same pattern several times reproduces precisely the same contraction shape: the B15/B16 -ARC neuromuscular transform is deterministic. However, varying the timing of the spikes produces very different contraction shapes and amplitudes. The transform in fact operates at an interface between "fast" and "slow" regimens. It is fast enough that the timing of individual spikes greatly influences the detailed contraction shape. At the same time, slow integration of the spike pattern through the nonlinear transform allows the variable spike timing to determine also the overall contraction amplitude. Indeed, the variability appears to be necessary to maintain the contraction amplitude at a robust level. This phenomenon is tuned by neuromodulators that tune the speed and nonlinearity of the transform. Thus, the variable timing of individual spikes does matter, in at least two, functionally significant ways, in this "slow" neuromuscular system.

Robot coverage control by evolved neuromodulation

“…A particularly applicable example in the realm of robotics is the neuromodulation of motor signals produced by central pattern generators in the brain and spinal cord [20]. It has been found that neuromodulators tune and synchronize neuromuscular signals [40].…”

Slow Temporal Filtering May Largely Explain the Transformation of Stick Insect (Carausius morosus) Extensor Motor Neuron Activity Into Muscle Movement

“…In particular, these data suggest that it may be worthwhile to determine whether the muscles in these other systems also have different time constants during contraction and relaxation. These muscles may also produce large shape transformations of their input, and simple models based primarily on slow temporal filtering again may be able to reproduce well these changes (although in Aplysia a strong history dependence on twitch amplitude would also need to be included; Zhurov and Brezina 2006). Such systems may also work exclusively or primarily within the dynamic domain of their governing equations.…”

“…Muscles often transform motor neuron activity into contraction in complex manners [for examples, see Aplysia feeding system (Brezina et al 2000;Zhurov and Brezina 2006), crustacean stomatogastric system (Morris and Hooper 1997, 1998, 2001Morris et al 2000;Thuma et al 2003), human (Lee et al 1999a,b;Thomas et al 1999), rat (Abbate et al 2000;Grottel and Celichowski 1999;Van Luteren and Sankey 2000), stick insect (Hooper et al 2006a,b)]. Understanding the neuromuscular transform is important because a major goal of neuroscience is understanding the neural basis of movement generation, and this goal cannot be achieved without understanding how muscles respond to their driving input.…”

Single Synapse Information Coding in Intraburst Spike Patterns of Central Pattern Generator Motor Neurons

“…Therefore, muscle contraction must be independent of information encoded in IBSPs. In contrast, in a different neuromuscular system (Zhurov and Brezina, 2006), the accessory radula closer muscle of Aplysia operates between the fast and slow regimens, presenting nonlinear contraction responses to different spike timings. The authors argue that such properties contribute to maintaining robust muscle contraction patterns in vivo.…”