Neural circuit flexibility in a small sensorimotor system

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Neuronal circuits underlying rhythmic behaviors (central pattern generators: CPGs) can generate rhythmic motor output without sensory input. However, sensory input is pivotal for generating behaviorally relevant CPG output. Here we discuss recent work in the decapod crustacean stomatogastric nervous system (STNS) identifying cellular and synaptic mechanisms whereby sensory inputs select particular motor outputs from CPG circuits. This includes several examples in which sensory neurons regulate the impact of descending projection neurons on CPG circuits. This level of analysis is possible in the STNS due to the relatively unique access to identified circuit, projection, and sensory neurons. These studies are also revealing additional degrees of freedom in sensorimotor integration that underlie the extensive flexibility intrinsic to rhythmic motor systems.

Highlights

► Neuronal circuits (CPGs) can generate rhythmic motor output without sensory input. ► Sensory input is pivotal for generating behaviorally relevant CPG output. ► We discuss cellular mechanisms whereby sensory inputs select different motor outputs. ► Sensory neurons can regulate the impact of projection neurons on CPG circuits. ► Degrees of freedom in sensorimotor integration enable flexibility in motor systems.

Introduction

In the isolated CNS, CPG circuits produce fictive motor patterns that resemble the rhythmic motor patterns underlying behaviors in the intact animal [1, 2, 3, 4, 5, 6]. However, the fictive pattern is generally not identical to the pattern in the behaving animal, partly due to the absence of sensory input in the isolated nervous system [7, 8, 9, 10, 11, 12, 13]. Sensory inputs often have phase-specific actions, but they can also have longer term actions on rhythmic motor systems, including activating or terminating motor patterns and modulating ongoing motor activity [2, 14, 15, 16, 17, 18]. Work in many systems, several of which are reviewed in this issue, continues to contribute to our understanding of sensorimotor integration. Here, we discuss recent work related to sensorimotor integration in the decapod crustacean STNS, with an emphasis on how sensory inputs select particular motor patterns from multifunctional motor circuits.

Section snippets

The stomatogastric system

The STNS has provided numerous insights into cellular, synaptic, and circuit mechanisms by which rhythmic motor patterns are generated and modulated, due to its accessibility and the ability to manipulate identified neurons at multiple levels of the system [1, 18, 19]. Many of these insights clearly resonate with recent work in other systems, although often it remains challenging in other systems to obtain a similarly detailed level of analysis [20, 21, 22, 23, 24, 25]. The STNS generates

Sensorimotor integration at the CPG and projection neuron levels

In the STNS and other motor systems, sensory inputs act at multiple levels, including onto motor neurons, CPG neurons, and projection neurons [1, 2, 14, 16, 27, 28] (Figure 1b). One well-documented sensory feedback pathway in the crab STNS that acts on CPG and projection neurons is the muscle stretch-sensitive gastropyloric receptors (GPRs), which provide both cycle-by-cycle regulation and longer term modulation (Figure 1a). The GPR dendrites are embedded in gastric mill protractor muscles and,

Sensorimotor gating

Sensory input is often locally regulated presynaptically, at sensory neuron axon terminals [28, 42, 43, 44, 45, 46]. Thus far, however, in few cases has the downstream impact of these actions been elucidated at the cellular, synaptic, and circuit levels. Recently, the impact of local gating of one sensory input by another sensory pathway at these multiple levels was determined in the lobster STNS [47••]. In this system, this gating action selectively downregulates the sensory synapse onto one

Sensory neuron specializations

Sensory neurons can have multiple spike initiation zones, as do other neuron types [28, 64, 65, 66, 67, 68]. One such STNS sensory neuron is AGR, which generates spontaneous low frequency tonic activity at a central spike initiation zone, and fires phasically at a relatively high frequency from its peripheral processes in response to muscle stretch and tension [62, 63, 69••] (Figure 4). Interestingly, the centrally initiated AGR spikes influence motor output even without sensory transduction,

Cotransmission

Cotransmission provides another level of complexity to sensorimotor integration, as to all aspects of neural signaling [26, 45, 77, 78, 79, 80, 81]. One well-studied multitransmitter sensory neuron is GPR, which contains serotonin (5HT), acetylcholine (ACh) and allatostatin (AST) peptide [29, 30, 31, 82]. GPR modulates the pyloric rhythm through distributed ionotropic and metabotropic actions on pyloric circuit neurons that involve at least 5HT and ACh [30, 31]. In contrast, the phasic GPR

Parallel sensory feedback

Most cellular-level studies have examined the impact of a single sensory pathway at a time. However, in the intact animal, convergent sensory signals likely occur regularly. Barriere et al. [47••] examined the convergent influence of two muscle sensory systems (AGR; posterior stomach receptors: PSRs) in the lobster STNS (Figure 3). Selectively stimulating AGR drives either of two gastric mill motor patterns, depending on the AGR firing rate [39]. The PSRs drive a single type of gastric mill

Conclusions/future directions

In vitro approaches have yielded considerable cellular-level information regarding the mechanisms underlying sensorimotor integration in rhythmic motor systems. The relatively unique access in the STNS to identified CPG neurons, sensory neurons, projection neurons and hormones has provided detailed cellular mechanisms, down to the level of independent regulation of cotransmitters and convergent actions on a single ionic current within a single neuron. Unexpected consequences for motor circuit

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgement

The work in our lab is supported by NIH grant NS29436.

References (90)

  • G. Barriere et al.

    Multiple mechanisms for integrating proprioceptive inputs that converge on the same motor pattern-generating network

    J Neurosci

    (2008)
  • D. Combes et al.

    Conditional dendritic oscillators in a lobster mechanoreceptor neurone

    J Physiol (Lond)

    (1997)
  • E. Marder et al.

    Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs

    Annu Rev Physiol

    (2007)
  • K.L. Briggman et al.

    Multifunctional pattern-generating circuits

    Annu Rev Neurosci

    (2008)
  • A.I. Selverston

    Invertebrate central pattern generator circuits

    Philos Trans R Soc Lond, B, Biol Sci

    (2010)
  • O.J. Mullins et al.

    Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems

    Prog Neurobiol

    (2010)
  • A. Borgmann et al.

    Sensory feedback induced by front-leg stepping entrains the activity of central pattern generators in caudal segments of the stick insect walking system

    J Neurosci

    (2009)
  • J. Ausborn et al.

    The interaction of positive and negative sensory feedback loops in dynamic regulation of a motor pattern

    J Comput Neurosci

    (2009)
  • M.P. Beenhakker et al.

    Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron

    J Neurosci

    (2005)
  • S.N. Zill et al.

    Neurobiology: reconstructing the neural control of leg coordination

    Curr Biol

    (2009)
  • A. Roberts et al.

    How neurons generate behavior in a hatchling amphibian tadpole: an outline

    Front Behav Neurosci

    (2010)
  • D.M. Blitz et al.

    Mechanosensory regulation of invertebrate motor systems

  • W. Stein

    Modulation of stomatogastric rhythms

    J Comp Physiol A Neuroethol Sens Neural Behav Physiol

    (2009)
  • M.P. Nusbaum et al.

    A small-systems approach to motor pattern generation

    Nature

    (2002)
  • E. Marder et al.

    Variability, compensation and homeostasis in neuron and network function

    Nat Rev Neurosci

    (2006)
  • G.W. Davis

    Homeostatic control of neural activity: from phenomenology to molecular design

    Annu Rev Neurosci

    (2006)
  • A. Berkowitz et al.

    Roles for multifunctional and specialized spinal interneurons during motor pattern generation in tadpoles, zebrafish larvae, and turtles

    Front Behav Neurosci

    (2010)
  • E. Marder et al.

    Multiple models to capture the variability in biological neurons and networks

    Nat Neurosci

    (2011)
  • G. Turrigiano

    Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement [Internet]

    Annu Rev Neurosci

    (2011)
  • O.J. Mullins et al.

    Local-distributed integration by a novel neuron ensures rapid initiation of animal locomotion

    J Neurophysiol

    (2011)
  • S. Rossignol et al.

    Dynamic sensorimotor interactions in locomotion

    Physiol Rev

    (2006)
  • P.S. Katz et al.

    Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells

    J Neurophysiol

    (1989)
  • P.S. Katz et al.

    Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents

    J Neurosci

    (1990)
  • P.S. Katz et al.

    Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion

    J Neurophysiol

    (1989)
  • N.D. DeLong et al.

    Presynaptic inhibition selectively weakens peptidergic cotransmission in a small motor system

    J Neurophysiol

    (2009)
  • D.M. Blitz et al.

    Different sensory systems share projection neurons but elicit distinct motor patterns

    J Neurosci

    (2004)
  • S.R. Saideman et al.

    Convergent motor patterns from divergent circuits

    J Neurosci

    (2007)
  • A.K. Friedman et al.

    Motor outputs in a multitasking network: relative contributions of inputs and experience-dependent network states

    J Neurophysiol

    (2009)
  • W.B. Kristan et al.

    Population coding and behavioral choice

    Curr Opin Neurobiol

    (1997)
  • U.B. Hedrich et al.

    Differential activation of projection neurons by two sensory pathways contributes to motor pattern selection

    J Neurophysiol

    (2009)
  • D. Combes et al.

    Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster

    J Neurosci

    (1999)
  • D.M. Blitz et al.

    A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons

    J Exp Biol

    (2008)
  • M.P. Beenhakker et al.

    Mechanosensory activation of a motor circuit by coactivation of two projection neurons

    J Neurosci

    (2004)
  • C.G. Evans et al.

    Regulation of spike initiation and propagation in an Aplysia sensory neuron: gating-in via central depolarization

    J Neurosci

    (2003)
  • R.A. DiCaprio

    Gating of afferent input by a central pattern generator

    J Neurophysiol

    (1999)
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