Neural circuit flexibility in a small sensorimotor system
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)
- et al.
Probing spinal circuits controlling walking in mammals
Biochem Biophys Res Commun
(2010) - et al.
Synaptically activated burst-generating conductances may underlie a group-pacemaker mechanism for respiratory rhythm generation in mammals
Prog Brain Res
(2010) - et al.
Measured motion: searching for simplicity in spinal locomotor networks
Curr Opin Neurobiol
(2009) Role of sensory feedback in the control of stance duration in walking cats
Brain Res Rev
(2008)- et al.
Organizing network action for locomotion: insights from studying insect walking
Brain Res Rev
(2008) - et al.
Zebrafish and motor control over the last decade
Brain Res Rev
(2008) - et al.
Initiation of locomotion in lampreys
Brain Res Rev
(2008) - et al.
Neuromodulation and the orchestration of the respiratory rhythm
Respir Physiol Neurobiol
(2008) - et al.
The roles of co-transmission in neural network modulation
Trends Neurosci
(2001) Using multi-neuron population recordings for neural prosthetics
Nat Neurosci
(2004)
Multiple mechanisms for integrating proprioceptive inputs that converge on the same motor pattern-generating network
J Neurosci
Conditional dendritic oscillators in a lobster mechanoreceptor neurone
J Physiol (Lond)
Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs
Annu Rev Physiol
Multifunctional pattern-generating circuits
Annu Rev Neurosci
Invertebrate central pattern generator circuits
Philos Trans R Soc Lond, B, Biol Sci
Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems
Prog Neurobiol
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
The interaction of positive and negative sensory feedback loops in dynamic regulation of a motor pattern
J Comput Neurosci
Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron
J Neurosci
Neurobiology: reconstructing the neural control of leg coordination
Curr Biol
How neurons generate behavior in a hatchling amphibian tadpole: an outline
Front Behav Neurosci
Mechanosensory regulation of invertebrate motor systems
Modulation of stomatogastric rhythms
J Comp Physiol A Neuroethol Sens Neural Behav Physiol
A small-systems approach to motor pattern generation
Nature
Variability, compensation and homeostasis in neuron and network function
Nat Rev Neurosci
Homeostatic control of neural activity: from phenomenology to molecular design
Annu Rev Neurosci
Roles for multifunctional and specialized spinal interneurons during motor pattern generation in tadpoles, zebrafish larvae, and turtles
Front Behav Neurosci
Multiple models to capture the variability in biological neurons and networks
Nat Neurosci
Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement [Internet]
Annu Rev Neurosci
Local-distributed integration by a novel neuron ensures rapid initiation of animal locomotion
J Neurophysiol
Dynamic sensorimotor interactions in locomotion
Physiol Rev
Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells
J Neurophysiol
Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents
J Neurosci
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
Presynaptic inhibition selectively weakens peptidergic cotransmission in a small motor system
J Neurophysiol
Different sensory systems share projection neurons but elicit distinct motor patterns
J Neurosci
Convergent motor patterns from divergent circuits
J Neurosci
Motor outputs in a multitasking network: relative contributions of inputs and experience-dependent network states
J Neurophysiol
Population coding and behavioral choice
Curr Opin Neurobiol
Differential activation of projection neurons by two sensory pathways contributes to motor pattern selection
J Neurophysiol
Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster
J Neurosci
A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons
J Exp Biol
Mechanosensory activation of a motor circuit by coactivation of two projection neurons
J Neurosci
Regulation of spike initiation and propagation in an Aplysia sensory neuron: gating-in via central depolarization
J Neurosci
Gating of afferent input by a central pattern generator
J Neurophysiol
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