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Abstract
The perception of proprioceptive signals that report the internal state of the body is one of the essential tasks of the nervous system and helps to continuously adapt body movements to changing circumstances. Despite the impact of proprioceptive feedback on motor activity it has rarely been studied in conditions in which motor output and sensory activity interact as they do in behaving animals, i.e., in closed-loop conditions. The interaction of motor and sensory activities, however, can create emergent properties that may govern the functional characteristics of the system. We here demonstrate a method to use a well-characterized model system for central pattern generation, the stomatogastric nervous system, for studying these properties in vitro. We created a real-time computer model of a single-cell muscle tendon organ in the gastric mill of the crab foregut that uses intracellular current injections to control the activity of the biological proprioceptor. The resulting motor output of a gastric mill motor neuron is then recorded intracellularly and fed into a simple muscle model consisting of a series of low-pass filters. The muscle output is used to activate a one-dimensional Hodgkin–Huxley type model of the muscle tendon organ in real-time, allowing closed-loop conditions. Model properties were either hand tuned to achieve the best match with data from semi-intact muscle preparations, or an exhaustive search was performed to determine the best set of parameters. We report the real-time capabilities of our models, its performance and its interaction with the biological motor system.
Highlights
The perception of proprioceptive signals that report the internal state of the body is one of the essential tasks of the nervous system, because it adapts ongoing motor activity to changes in the environment or the body
The gastric mill central pattern generator in the stomatogastric ganglion (STG) has been studied in great detail (Bartos and Nusbaum, 1997; Nusbaum and Beenhakker, 2002; Stein et al, 2007; Stein, 2009)
Its connectivity and cellular components are well-characterized, as are sensory feedback pathways (Katz and Harris-Warrick, 1989; Katz et al, 1989; Katz, 1998; Birmingham, 2001; Birmingham and Tauck, 2003; Beenhakker et al, 2004, 2005; Blitz et al, 2004, 2008; Billimoria et al, 2006; Le et al, 2006; Barriere et al, 2008) and muscle properties (Jorge-Rivera and Marder, 1996; Jorge-Rivera et al, 1998; Stein et al, 2006). This makes this system attractive to test the effect of realistic closed-loop proprioceptive feedback on motor pattern generation
Summary
The perception of proprioceptive signals that report the internal state of the body is one of the essential tasks of the nervous system, because it adapts ongoing motor activity to changes in the environment or the body (review in Pearson, 1986; Grillner, 2003; Pearson, 2004). Phasic proprioceptive feedback contributes significantly to the motor output in many rhythmic motor systems (Rossignol et al, 2006; Ausborn et al, 2007). It is often regarded as an integral part of the rhythm generating machinery (Pearson, 2004), even if the basic motor pattern can still be expressed after removing all sensory input. The dynamical components determined by the interaction of motor and sensory activities can create emergent properties that govern the functional characteristics of the system (Lehmann and Dickinson, 2000; Büschges, 2005). In the few instances in which they have been studied (Bässler and Nothof, 1994; Ausborn et al, 2007, 2009; Smarandache et al, 2008), it is obvious that they play an important role in shaping the motor output
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