Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crabCancer pagurus

Abstract

Hedrich UB, Diehl F, Stein W. Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crab Cancer pagurus. J Neurophysiol 105: 1671-1680, 2011. First published February 16, 2011 doi:10.1152/jn.01105.2010.-Neuronal release of modulatory substances provides motor pattern generating circuits with a high degree of flexibility. In vitro studies have characterized the actions of modulatory projection neurons in great detail in the stomatogastric nervous system, a model system for neuromodulatory influences on central pattern generators. Less is known about the activities and actions of modulatory neurons in fully functional and richly modulated network settings, i.e., in intact animals. It is also unknown whether their activities contribute to the motor patterns in different behavioral conditions. Here, we show for the first time the activity and effects of the well-characterized modulatory projection neuron 1 (MCN1) in vivo and compare them to in vitro conditions. MCN1 was always spontaneously active, typically in a rhythmic fashion with its firing being interrupted by ascending inhibitions from the pyloric motor circuit. Its activity contributed to pyloric motor activity, because 1) the cycle period of the motor pattern correlated with MCN1 firing frequency and 2) stimulating MCN1 shortened the cycle period while 3) lesioning of the MCN1 axon reduced motor activity. In addition, gastric mill motor activity was elicited for the duration of the stimulation. Chemosensory stimulation of the antennae moved MCN1 away from baseline activity by increasing its firing frequency. Following this increase, a gastric mill rhythm was elicited and the pyloric cycle period decreased. Lesioning the MCN1 axon prevented these effects. Thus modulatory projection neurons such as MCN1 can control the motor output in vivo, and they participate in the processing of exteroceptive sensory information in behaviorally relevant conditions. stomatogastric nervous system; central pattern generator; sensorimotor; descending control; neuromodulation ONE OF THE BIGGEST CHALLENGES today is to determine how the neuromodulatory system contributes to the neuronal plasticity that allows the nervous system to respond adequately to different behavioral tasks (Gu 2002;Calabrese 2003;Krichmar 2008;Brezina 2010). In particular, motor pattern generating circuits show a high degree of flexibility due to neuromodulatory substances that trigger new patterns or modify ongoing activity (Morgan et al. 2002;Nusbaum and Beenhakker 2002;Marder et al. 2005;Dickinson 2006;Sakurai and Katz 2009). Recent studies (Chen et al. 2009) have addressed the complexity and variety of paracrine neuromodulator release in vivo, but much less is known about the in vivo activity of neuromodulatory neurons that control behavior. In general, motor networks are governed by descending neurons from higher order circuits that are involved in decision making or relay the appropriate decisive information. In lamprey, fish, and tadpole, reticulospinal neurons in...

Sources and range of long-term variability of rhythmic motor patternsin vivo.

“…We found that in unfed animals, the phase relationships of the pyloric neurons rarely deviated from the canonical patterns, indicating that the pyloric rhythm's structure remains stable. This was despite several studies showing that, in vivo, the STG is continuously exposed to both hormonal and neural modulation (Diehl et al, 2013;Hedrich et al, 2011;Behrens et al, 2008;Schmerberg and Li, 2013;Christie et al, 1995), which have the potential to modify the phase relationships of the involved motor neurons (Marder and Weimann, 1992).…”

“…Accordingly, STG activity should be modulated by neuronal modulation as well as hormonal modulation. Curiously, however, despite stimulation of descending projection neurons both in vitro (Nusbaum and Beenhakker, 2002) and in vivo (Diehl et al, 2013;Hedrich et al, 2011) resulting in clear changes of CPG activity, most reported in vivo data show only the canonical motor patterns typically observed in unperturbed in vitro preparations (Hedrich et al, 2011;Massabuau and Meyrand, 1996;Clemens et al, 1998b). This is in spite of there being clear changes in the STG motor output in vitro Marder and Calabrese, 1996) and in vivo (Heinzel, 1988) in response to application of modulators known to be present in the blood (Li et al, 2002;Chen et al, 2009).…”

“…In particular, the range of variation in cycle frequency and phase relationships, as well as the range in response to various external and internal influences that these rhythms display is mostly unclear (Heinzel et al, 1993;Hedrich et al, 2011;Diehl et al, 2013;Soofi et al, 2014). For example, the in vivo activity patterns described so far for the pyloric rhythm (Soofi et al, 2014;Clemens et al, 1998a,b) reflect the canonical pyloric pattern, but show no signs of the expected plasticity inferred from neuromodulation experiments in the isolated system.…”

Muscles innervated by a single motor neuron exhibit divergent synaptic properties on multiple time scales

“…The single firing rate (10 Hz=100 ms inter-spike interval) and burst duration (4.8 s) used were also within the physiological range of LG activity (inter-spike interval: 50-250 ms; burst duration: 2-9 s) (Beenhakker et al, 2004(Beenhakker et al, , 2005(Beenhakker et al, , 2007Blitz et al, 2004bBlitz et al, , 2008Colton and Nusbaum, 2014;DeLong and Nusbaum, 2010;Diehl et al, 2013;Hedrich et al, 2011;Kirby and Nusbaum, 2007;White and Nusbaum, 2011). Thus, our data indicate that during gastric mill rhythms triggered by multiple inputs, augmentation and facilitation/ depression would regulate responses of the three target muscles of LG.…”

“…Diehl et al (2013) focused on distinctions in the pattern of spiking within LG bursts, but a number of other aspects of LG activity differ depending on modulatory state and the complement of inputs acting on LG. In response to a number of different modulatory inputs, LG activity consists of firing rates of 4-20 Hz (50-250 ms inter-spike intervals), burst durations of 2-8 s and interburst intervals of 2-24 s in vitro and in vivo (Beenhakker et al, 2004(Beenhakker et al, , 2005(Beenhakker et al, , 2007Blitz et al, 2004bBlitz et al, , 2008Colton and Nusbaum, 2014;DeLong and Nusbaum, 2010;Diehl et al, 2013;Hedrich et al, 2011;Kirby and Nusbaum, 2007;White and Nusbaum, 2011). Similar to central and peripheral synapses in other systems, electrical responses at neuromuscular junctions in the STNS are shaped by multiple forms of activity-dependent synaptic plasticity including depression, facilitation and augmentation (Daur et al, 2012b;Jorge-Rivera et al, 1998;Katz et al, 1993;Sen et al, 1996;Stein et al, 2006).…”