Neural circuit flexibility in a small sensorimotor system

Blitz, Dawn M.; Nusbaum, Michael P.

doi:10.1016/j.conb.2011.05.019

Cited by 71 publications

(57 citation statements)

References 88 publications

(155 reference statements)

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“…In the other cases, they always saw a clear effect on period and they interpreted this difference to stimulating a different command neuron. Similar effects can be observed in the crustacean stomatogastric system, where sensory feedback interacts with projecting neurons to produce different styles of motor output (Blitz and Nusbaum, 2011). …”

Section: Proprioceptive Reflexes and Sensorimotor Integrationsupporting

confidence: 52%

Neurobiology of the crustacean swimmeret system

Mulloney

Smarandache‐Wellmann

2012

Progress in Neurobiology

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The crustacean swimmeret system includes a distributed set of local circuits that individually control movements of one jointed limb. These modular local circuits occur in pairs in each segmental ganglion, and normally operate synchronously to produce smoothly coordinated cycles of limb movements on different body segments. The system presents exceptional opportunities for computational and experimental investigation of neural mechanisms of coordination because: a. The system will express in vitro the periodic motor pattern that normally drives cycles of swimmeret movements during forward swimming. b. The intersegmental neurons which encode information that is necessary and sufficient for normal coordination have been identified, and their activity can be recorded. c. The local commissural neurons that integrate this coordinating information and tune the phase of each swimmeret are known. d. The complete set of synaptic connections between coordinating neurons and these commissural neurons have been described. e. The synaptic connections onto each local pattern-generating circuit through which coordinating information tunes the circuit's phase have been discovered. These factors make possible for the first time a detailed, comprehensive cellular and synaptic explanation of how this neural circuit produces an effective, behaviorally-significant output. This paper is the first comprehensive review of the system's neuroanatomy and neurophysiology, its local and intersegmental circuitry, its transmitter pharmacology, its neuromodulatory control mechanisms, and its interactions with other motor systems. Each of these topics is covered in detail in an attempt to provide a complete review of the literature as a foundation for new research. The series of hypotheses that have been proposed to account for the system's properties are reviewed critically in the context of experimental tests of their validity.

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Section: Proprioceptive Reflexes and Sensorimotor Integrationsupporting

confidence: 52%

Neurobiology of the crustacean swimmeret system

Mulloney

Smarandache‐Wellmann

2012

Progress in Neurobiology

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“…Although this may seem surprising on comparison with Ciona , it should be less unexpected in a broader context. For example, the stomatogastric ganglion of crustaceans, containing only about 30 neurons, is capable of producing diverse rhythmic motor outputs, a consequence of various modulatory mechanisms including ongoing circuit remodeling through the actions of neurotransmitters and hormones and their interactions with sensory inputs [Stein, 2009;Blitz and Nusbaum, 2011]. Thus, despite having only 20 muscle cells, 20 motoneurons, and no more than about 45 additional neurons within the caudal ganglion and caudal nerve cord, Oikopleura clearly manages to differentially sculpt motor output according to different requirements, either through similar modulatory mechanisms or, perhaps more likely, through switching among alternative dynamic states .…”

Section: Complexity Of the Behavioral Repertoirementioning

confidence: 99%

Developmental Characterization of Tail Movements in the Appendicularian Urochordate <b><i>Oikopleura dioica</i></b>

Kréneisz

Glover²

2015

Brain Behav Evol

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Using high-speed video cinematography, we characterized kinematically the spontaneous tail movements made by the appendicularian urochordate Oikopleura dioica. Videos of young adult (1-day-old) animals discriminated 4 cardinal movement types: bending, nodding, swimming and filtering, each of which had a characteristic signature including cyclicity, event or cycle duration, cycle frequency, cycle frequency variation, laterality, tail muscle segment coordination and episode duration. Bending exhibited a more common, unilateral form (single bending) and a rarer, bilateral form (alternating bending). Videos of developing animals showed that bending and swimming appeared in rudimentary form starting just after hatching and exhibited developmental changes in movement excursion, duration and frequency, whereas nodding and filtering appeared in the fully mature form in young adults at the time of first house production. More complex behaviors were associated with inflating, entering and exiting the house. We also assessed the influence of descending inputs by separating the tail (which contains all muscles and most likely the neural circuits that generate most motor outputs) from the head. Isolated tails spontaneously generated either bending or swimming movements in abnormally protracted episodes. This together with other observations of interactions between bending and swimming behaviors indicates the presence of several types of descending inputs that regulate the activity of the pattern generating circuitry in the tail nervous system.

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“…Both CPG circuits in the STG have been characterized in great detail [18], [21], [22] using mostly traditional extra- and intracellular electrophysiology after desheathing. The gastric mill CPG is influenced by sensory pathways, such as the proprioceptive anterior gastric receptor (AGR, [23]).…”

Section: Introductionmentioning

confidence: 99%

Optical Imaging of Neuronal Activity and Visualization of Fine Neural Structures in Non-Desheathed Nervous Systems

2014

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Locating circuit neurons and recording from them with single-cell resolution is a prerequisite for studying neural circuits. Determining neuron location can be challenging even in small nervous systems because neurons are densely packed, found in different layers, and are often covered by ganglion and nerve sheaths that impede access for recording electrodes and neuronal markers. We revisited the voltage-sensitive dye RH795 for its ability to stain and record neurons through the ganglion sheath. Bath-application of RH795 stained neuronal membranes in cricket, earthworm and crab ganglia without removing the ganglion sheath, revealing neuron cell body locations in different ganglion layers. Using the pyloric and gastric mill central pattern generating neurons in the stomatogastric ganglion (STG) of the crab, Cancer borealis, we found that RH795 permeated the ganglion without major residue in the sheath and brightly stained somatic, axonal and dendritic membranes. Visibility improved significantly in comparison to unstained ganglia, allowing the identification of somata location and number of most STG neurons. RH795 also stained axons and varicosities in non-desheathed nerves, and it revealed the location of sensory cell bodies in peripheral nerves. Importantly, the spike activity of the sensory neuron AGR, which influences the STG motor patterns, remained unaffected by RH795, while desheathing caused significant changes in AGR activity. With respect to recording neural activity, RH795 allowed us to optically record membrane potential changes of sub-sheath neuronal membranes without impairing sensory activity. The signal-to-noise ratio was comparable with that previously observed in desheathed preparations and sufficiently high to identify neurons in single-sweep recordings and synaptic events after spike-triggered averaging. In conclusion, RH795 enabled staining and optical recording of neurons through the ganglion sheath and is therefore both a good anatomical marker for living neural tissue and a promising tool for studying neural activity of an entire network with single-cell resolution.

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Neural circuit flexibility in a small sensorimotor system

Cited by 71 publications

References 88 publications

Neurobiology of the crustacean swimmeret system

Neurobiology of the crustacean swimmeret system

Developmental Characterization of Tail Movements in the Appendicularian Urochordate <b><i>Oikopleura dioica</i></b>

Optical Imaging of Neuronal Activity and Visualization of Fine Neural Structures in Non-Desheathed Nervous Systems

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