Feedback to the future: motor neuron contributions to central pattern generator function.
TL;DR: This Review discusses literature examining the role of motor neuron feedback across many taxa and behaviors, and sets out to determine the prevalence of motor neurons participation in motor circuits.
Abstract: Motor behaviors depend on neural signals in the brain. Regardless of where in the brain behavior patterns arise, the central nervous system sends projections to motor neurons, which in turn project to and control temporally appropriate muscle contractions; thus, motor neurons are traditionally considered the last relay from the central nervous system to muscles. However, in an array of species and motor systems, an accumulating body of evidence supports a more complex role of motor neurons in pattern generation. These studies suggest that motor neurons not only relay motor patterns to the periphery, but directly contribute to pattern generation by providing feedback to upstream circuitry. In spinal and hindbrain circuits in a variety of animals - including flies, worms, leeches, crustaceans, rodents, birds, fish, amphibians and mammals - studies have indicated a crucial role for motor neuron feedback in maintaining normal behavior patterns dictated by the activity of a central pattern generator. Hence, in this Review, we discuss literature examining the role of motor neuron feedback across many taxa and behaviors, and set out to determine the prevalence of motor neuron participation in motor circuits.
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TL;DR: Xenopus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution, as one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems.
Abstract: In many species, vocal communication is essential for coordinating social behaviors including courtship, mating, parenting, rivalry, and alarm signaling. Effective communication requires accurate production, detection, and classification of signals, as well as selection of socially appropriate responses. Understanding how signals are generated and how acoustic signals are perceived is key to understanding the neurobiology of social behaviors. Here we review our long-standing research program focused on Xenopus, a frog genus which has provided valuable insights into the mechanisms and evolution of vertebrate social behaviors. In Xenopus laevis, vocal signals differ between the sexes, through development, and across the genus, reflecting evolutionary divergence in sensory and motor circuits that can be interrogated mechanistically. Using two ex vivo preparations, the isolated brain and vocal organ, we have identified essential components of the vocal production system: the sexually differentiated larynx at the periphery, and the hindbrain vocal central pattern generator (CPG) centrally, that produce sex- and species-characteristic sound pulse frequencies and temporal patterns, respectively. Within the hindbrain, we have described how intrinsic membrane properties of neurons in the vocal CPG generate species-specific vocal patterns, how vocal nuclei are connected to generate vocal patterns, as well as the roles of neurotransmitters and neuromodulators in activating the circuit. For sensorimotor integration, we identified a key forebrain node that links auditory and vocal production circuits to match socially appropriate vocal responses to acoustic features of male and female calls. The availability of a well supported phylogeny as well as reference genomes from several species now support analysis of the genetic architecture and the evolutionary divergence of neural circuits for vocal communication. Xenopus thus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution. As one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems, Xenopus provides insights that can inform social communication across phyla.
24 citations
Cites background or result from "Feedback to the future: motor neuro..."
...In either case, results of vocal motor neuron inactivation show that motor neurons are part of the Xenopus vocal CPG as for other CPGs across taxa (Lawton et al., 2017; Barkan and Zornik, 2019)....
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...Whereas motor neurons in invertebrates are known to play key roles in pattern generation, in vertebrates they are more typically considered to be relays between the upstream neural circuitry and muscles (for review, see Barkan and Zornik, 2019)....
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...…model (Yamaguchi et al., 2017) is that the hindbrain CPG for advertisement calling includes NA in the posterior hindbrain, the parabrachial nucleus in the anterior hindbrain as well as a recurrent contribution originating from vocal motor neurons (Lawton et al., 2017; Barkan and Zornik, 2019; Fig....
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TL;DR: In this paper, a multaceted mass spectrometry (MS) method was used to identify neuropeptides that differentiate the unfed and fed states in the crab Cancer borealis nervous system.
Abstract: The crab Cancer borealis nervous system is an important model for understanding neural circuit dynamics and modulation, but the identity of neuromodulatory substances and their influence on circuit dynamics in this system remains incomplete, particularly with respect to behavioral state-dependent modulation. Therefore, we used a multifaceted mass spectrometry (MS) method to identify neuropeptides that differentiate the unfed and fed states. Duplex stable isotope labeling revealed that the abundance of 80 of 278 identified neuropeptides was distinct in ganglia and/or neurohemal tissue from fed vs unfed animals. MS imaging revealed that an additional 7 and 11 neuropeptides exhibited altered spatial distributions in the brain and the neuroendocrine pericardial organs (POs), respectively, during these two feeding states. Furthermore, de novo sequencing yielded 69 newly identified putative neuropeptides that may influence feeding state-related neuromodulation. Two of these latter neuropeptides were determined to be upregulated in PO tissue from fed crabs, and one of these two peptides influenced heartbeat in ex vivo preparations. Overall, the results presented here identify a cohort of neuropeptides that are poised to influence feeding-related behaviors, providing valuable opportunities for future functional studies.
14 citations
TL;DR: A taxonomic review of the family Tritoniidae using integration of molecular phylogenetic analysis, morphological and biogeographical data, showing that Tochuina possesses specialized tritoniid features and also some characters of “arminacean nudibranchs”, such as Doridoxa and Heterodoris.
Abstract: Nudibranch molluscs of the family Tritoniidae are widely used neuroscience model systems for understand the behavioural and genetic bases of learning and memory. However species identity and genus-level taxonomic assignment of the tritoniids remain contested. Herein we present a taxonomic review of the family Tritoniidae using integration of molecular phylogenetic analysis, morphological and biogeographical data. For the first time the identity of the model species Tritonia tetraquetra (Pallas, 1788) and Tritonia exsulans Bergh, 1894 is confirmed. T. tetraquetra distributes across the large geographic and bathymetric distances in the North-Eastern (NE) and North-Western (NW) Pacific. In turn, at NE Pacific coasts the separate species T. exsulans is commonly occured. Thus, it reveals a misidentification of T. tetraquetra and T. exsulans species in neuroscience applications. Presence of more hidden lineages within NW Pacific T. tetraquetra is suggested. The long lasting confusion over identity of the species from the genera Tritonia and Tochuina is resolved using molecular and morphological data. We also disprove a common indication about "edible T. tetraquetra" at the Kuril Islands. It is shown that Tochuina possesses specialized tritoniid features and also some characters of "arminacean nudibranchs", such as Doridoxa and Heterodoris. Diagnoses for the families Doridoxidae and Heterodorididae are provided. Taxonomy of the genus Doridoxa is clarified and molecular data for the genus Heterodoris presented for the first time. A taxonomic synopsis for the family Tritoniidae is provided. A new genus among tritoniid taxa is proposed. Importance of the ontogeny-based taxonomy is highlighted. The cases when apomorphic characters considerably modified in a crown group due to the paedomorphosis are revealed. Tracing of the character evolution is presented for secondary gills-a key external feature of the family Tritoniidae and traditional dendronotacean nudibranchs.
11 citations
TL;DR: Brainstem mechanisms controlling locomotion, together with indirect evidence from human electrophysiologic and functional neuroimaging studies, provides testable pathophysiologic hypotheses and potential therapeutic targets for gait control disorders.
Abstract: Locomotion in humans is defined as bipedal progression through stages of a gait cycle to move from one place to another while maintaining balance and posture. Locomotion can be categorized in temporal phases (initiation, actual locomotive episode/execution, and termination) or in behavioral categories (slow exploratory and fast speed locomotion). The motivation behind a locomotive episode may be driven by internal needs (goal driven from the motor cortex or emotion driven from the limbic system) or external environmental cues. Locomotion is mediated by a spinal central pattern generator (CPG) under the influence of the brainstem reticular formation and is integrated with control of muscle tone and posture. Control of gait, muscle tone, and posture involves complex interactions among the sensorimotor cortex, basal ganglia, basal forebrain, cerebellum, brainstem, and spinal cord.1-3 Pioneering studies in cats4 and monkeys5,6 and more recently in rodents7-12 have contributed to elucidate the brainstem mechanisms controlling locomotion. This information, together with indirect evidence from human electrophysiologic and functional neuroimaging studies, provides testable pathophysiologic hypotheses and potential therapeutic targets for gait control disorders. The focus of this review is on brainstem mechanisms controlling locomotion. The role of other CNS areas in control of gait and posture and their abnormalities in disorders such as Parkinson disease (PD) have been extensively reviewed1 and are only briefly discussed here.
6 citations
TL;DR: In this article, gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation was shown to provide a timing mechanism for achieving synchrony and temporal precision for rapid modulation of acoustic waveforms.
Abstract: Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchronous motoneuron firing within a hindbrain network directly determining the temporal structure of natural calls. Here, we investigated how these motoneurons maintain synchronous activation. We show that pronounced temporal precision in population-level motoneuronal firing depends on gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites formed by a subset of adjacent premotoneurons contacting motoneuron somata and dendrites. In aggregate, the evidence supports the hypothesis that gap junction-mediated, glycinergic inhibition provides a timing mechanism for achieving synchrony and temporal precision in the millisecond range for rapid modulation of acoustic waveforms.
6 citations
References
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TL;DR: The structure and connectivity of the nervous system of the nematode Caenorhabditis elegans has been deduced from reconstructions of electron micrographs of serial sections as discussed by the authors.
Abstract: The structure and connectivity of the nervous system of the nematode Caenorhabditis elegans has been deduced from reconstructions of electron micrographs of serial sections. The hermaphrodite nervous system has a total complement of 302 neurons, which are arranged in an essentially invariant structure. Neurons with similar morphologies and connectivities have been grouped together into classes; there are 118 such classes. Neurons have simple morphologies with few, if any, branches. Processes from neurons run in defined positions within bundles of parallel processes, synaptic connections being made en passant. Process bundles are arranged longitudinally and circumferentially and are often adjacent to ridges of hypodermis. Neurons are generally highly locally connected, making synaptic connections with many of their neighbours. Muscle cells have arms that run out to process bundles containing motoneuron axons. Here they receive their synaptic input in defined regions along the surface of the bundles, where motoneuron axons reside. Most of the morphologically identifiable synaptic connections in a typical animal are described. These consist of about 5000 chemical synapses, 2000 neuromuscular junctions and 600 gap junctions.
5,491 citations
TL;DR: Cellular, circuit, and computational analyses of the mechanisms underlying the generation of rhythmic movements in both invertebrate and vertebrate nervous systems are discussed.
Abstract: Rhythmic movements are produced by central pattern-generating networks whose output is shaped by sensory and neuromodulatory inputs to allow the animal to adapt its movements to changing needs. This review discusses cellular, circuit, and computational analyses of the mechanisms underlying the generation of rhythmic movements in both invertebrate and vertebrate nervous systems. Attention is paid to exploring the mechanisms by which synaptic and cellular processes interact to play specific roles in shaping motor patterns and, consequently, movement.
1,275 citations
"Feedback to the future: motor neuro..." refers background in this paper
...CPGs are experimentally powerful because they can often be activated and studied in isolated brains, producing ‘fictive behaviors’ (see Glossary) in which circuit output closely resembles naturally observed behavior patterns (Marder and Calabrese, 1996)....
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...Over the next several decades, neurobiologists began studying the CPGs underlying a variety of motor behaviors, and it is now accepted that CPGs underlie most, if not all, rhythmic behaviors (Goulding, 2009; Marder and Bucher, 2007; Marder and Calabrese, 1996)....
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TL;DR: During phasic acts the dynamic balance of the neural centres is disturbed by two different kinds of peripheral stimuli that produce changes in the activity of exteroceptive end-organs therein embedded, and discontinuous augmentations and diminutions of the stimuli originated in them.
Abstract: Whilst the act of progression is being performed, the several limbs exhibit rhythmic movements of flexion and of extension. When any limb is in contact with the ground, it extends, and thus serves to propel the animal forwards. At the end of this act the limb is lifted from the ground by a movement of flexion, is carried forward, and finally is again placed upon the ground to repeat the cycle. During these phasic acts the dynamic balance of the neural centres is disturbed by two different kinds of peripheral stimuli. In the first place, the discontinuous contact with the ground, and the synchronous distortion of the skin of the foot—determined by the weight of the animal then carried in part by that limb—produce changes in the activity of exteroceptive end-organs therein embedded, and discontinuous augmentations and diminutions of the stimuli originated in them.
1,196 citations
"Feedback to the future: motor neuro..." refers background in this paper
...Thomas Graham Brown (1882–1965), Anders Lundberg (1920–), and the neural control of stepping....
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...Origins of CPG theories Thomas Graham Brown (1911) performed experiments in which signals to the cat spinal cord – both descending inputs from the brain and sensory inputs from the periphery – were eliminated; these cats remained able to produce rhythmic stepping behavior, suggesting the presence…...
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...Origins of CPG theories Thomas Graham Brown (1911) performed experiments in which signals to the cat spinal cord – both descending inputs from the brain and sensory inputs from the periphery – were eliminated; these cats remained able to produce rhythmic stepping behavior, suggesting the presence of intrinsic oscillating circuits located in the spinal cord....
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1,191 citations
TL;DR: The wiring diagram reported here can help in understanding the mechanistic basis of behavior by generating predictions about future experiments involving genetic perturbations, laser ablations, or monitoring propagation of neuronal activity in response to stimulation.
Abstract: Despite recent interest in reconstructing neuronal networks, complete wiring diagrams on the level of individual synapses remain scarce and the insights into function they can provide remain unclear. Even for Caenorhabditis elegans, whose neuronal network is relatively small and stereotypical from animal to animal, published wiring diagrams are neither accurate nor complete and self-consistent. Using materials from White et al. and new electron micrographs we assemble whole, self-consistent gap junction and chemical synapse networks of hermaphrodite C. elegans. We propose a method to visualize the wiring diagram, which reflects network signal flow. We calculate statistical and topological properties of the network, such as degree distributions, synaptic multiplicities, and small-world properties, that help in understanding network signal propagation. We identify neurons that may play central roles in information processing, and network motifs that could serve as functional modules of the network. We explore propagation of neuronal activity in response to sensory or artificial stimulation using linear systems theory and find several activity patterns that could serve as substrates of previously described behaviors. Finally, we analyze the interaction between the gap junction and the chemical synapse networks. Since several statistical properties of the C. elegans network, such as multiplicity and motif distributions are similar to those found in mammalian neocortex, they likely point to general principles of neuronal networks. The wiring diagram reported here can help in understanding the mechanistic basis of behavior by generating predictions about future experiments involving genetic perturbations, laser ablations, or monitoring propagation of neuronal activity in response to stimulation.
746 citations
"Feedback to the future: motor neuro..." refers background in this paper
...Innovative efforts in the nematode Caenorhabditis elegans gave us the first complete wiring diagram of a nervous system, in which motor neurons were shown to form both chemical and electrical synapses (see Glossary) with interneurons (Varshney et al., 2011; White et al., 1986)....
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...elegans and Ciona intestinalis) revealed motor neuron connections to CNS neurons (Ryan et al., 2016; Varshney et al., 2011; White et al., 1986)....
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