Chick spinal accessory lobes contain functional neurons expressing voltagegated sodium channels generating action potentials

Yamanaka, Yuko; Naoki, Katsuhiko; Shibuya, Izumi

doi:10.2220/biomedres.29.205

Cited by 11 publications

(8 citation statements)

References 17 publications

(24 reference statements)

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“…The LSO presents a suite of features unique to the spinal column of birds, including bilateral protrusions of neural tissue identified as mechanosensors (accessory lobe (AL) neurons), located adjacent to ligaments supporting the spinal cord (Schroeder and Murray, 1987;Necker, 2005Necker, , 2006Yamanaka et al, 2008). The spinal cord is dorsally bifurcated in this region and supports a "glycogen body" (GB) centered on top.…”

Section: Introductionmentioning

confidence: 99%

“…The arrangement of the canals, AL, ligaments, and GB is reminiscent of the vestibular system (Necker, 2006) and invites functional analogy to an accelerometer. Each AL contains mechanoreceptors (Schroeder and Murray, 1987;Necker, 2006;Yamanaka et al, 2008), with commissural axons projecting to last-order premotor interneurons in the spinal pattern generating network (Eide and Glover, 1996;Necker, 2006). The AL neurons within the LSO exhibit spontaneous firing and phase-coupled firing in response to vibrational stimulation between 75 and 100 Hz, and ablation of these neurons disrupts standing balance (Necker, 2006).…”

Section: Introductionmentioning

confidence: 99%

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A Physical Model Suggests That Hip-Localized Balance Sense in Birds Improves State Estimation in Perching: Implications for Bipedal Robots

et al. 2018

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In addition to a vestibular system, birds uniquely have a balance-sensing organ within the pelvis, called the lumbosacral organ (LSO). The LSO is well developed in terrestrial birds, possibly to facilitate balance control in perching and terrestrial locomotion. No previous studies have quantified the functional benefits of the LSO for balance. We suggest two main benefits of hip-localized balance sense: reduced sensorimotor delay and improved estimation of foot-ground acceleration. We used system identification to test the hypothesis that hip-localized balance sense improves estimates of foot acceleration compared to a head-localized sense, due to closer proximity to the feet. We built a physical model of a standing guinea fowl perched on a platform, and used 3D accelerometers at the hip and head to replicate balance sense by the LSO and vestibular systems. The horizontal platform was attached to the end effector of a 6 DOF robotic arm, allowing us to apply perturbations to the platform analogous to motions of a compliant branch. We also compared state estimation between models with low and high neck stiffness. Cross-correlations revealed that foot-to-hip sensing delays were shorter than foot-to-head, as expected. We used multi-variable output error state-space (MOESP) system identification to estimate foot-ground acceleration as a function of hip-and head-localized sensing, individually and combined. Hip-localized sensors alone provided the best state estimates, which were not improved when fused with head-localized sensors. However, estimates from head-localized sensors improved with higher neck stiffness. Our findings support the hypothesis that hip-localized balance sense improves the speed and accuracy of foot state estimation compared to head-localized sense. The findings also suggest a role of neck muscles for active sensing for balance control: increased neck stiffness through muscle co-contraction can improve the utility of vestibular signals. Our engineering approach provides, to our knowledge, the first quantitative evidence for functional benefits of the LSO balance sense in birds. The Urbina-Meléndez et al.Hip Balance-Sense Implications Bipedal Robots findings support notions of control modularity in birds, with preferential vestibular sense for head stability and gaze, and LSO for body balance control,respectively. The findings also suggest advantages for distributed and active sensing for agile locomotion in compliant bipedal robots.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A Physical Model Suggests That Hip-Localized Balance Sense in Birds Improves State Estimation in Perching: Implications for Bipedal Robots

et al. 2018

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“…Previously, we found that enzymatically isolated cells from ALs of chick embryos showed depolarization-activated Na + current in the electrophysiological recording (18). In addition, it was reported that an intracellular concentration of Cl − in neuron-like cells isolated from chick embryonic ALs was as low as that of neurons of adult chicks (19), suggesting that a developing stage of neurons of chick embryos at E16-18 is similar to that of adult animals.…”

Section: Discussionmentioning

confidence: 90%

“…Subsequently, the supernatant was centrifuged again at 8,000 × g for 10 min rotransmitters exist in the ALs (9,12,13), there is little cellular evidence indicating that AL cells have neuronal functions. Previously, we reported that cells isolated from chick ALs showed voltage-gated Na + and K + currents under voltage-clamp conditions and generated action potentials under current-clamp conditions in whole-cell patch-clamp experiments (18). These results indicate that the voltage-gated Na + channel (VGSC) is expressed and that functional neurons generating action potentials exist in ALs.…”

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confidence: 74%

<b>Neuron-like cells in the chick spinal accessory lobe express neuronal-type voltage-gated sodium </b><b>channels </b>

et al. 2018

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Ten pairs of protrusions, called accessory lobes (ALs), exist at the lateral sides of the avian lumbosacral spinal cord. Histological evidence indicates that neuron-like cells gather in the ALs, and behavioral evidence suggests that the ALs act as a sensory organ of equilibrium during bipedal walking. Recently, using an electrophysiological method, we reported that cells showing Na currents and action potentials exist among cells that were dissociated from the ALs. However, it was unclear which isoforms of the voltage-gated sodium channel (VGSC) are expressed in the ALs and whether cells having neuronal morphology in the ALs express VGSCs. To elucidate these points, RT-PCR and immunohistochemical experiments were performed. In RT-PCR analysis, PCR products for Na 1.1-1.7 were detected in the ALs. The signal intensities of the Na 1.1 and 1.6 isoforms were stronger than those of the other isoforms. We confirmed that an antibody raised against an epitope peptide of the rat VGSC had cross-reactivity to chick tissues by Western blotting, and we performed immunofluorescence staining using the antibody. The AL contained cells having neuron-like morphology and VGSC-like immunoreactivity at their cytoplasm and/or cell membranes. Filament-like structures showing GFAP-like immunoreactivity infilled intercellular spaces. The VGSC- and GFAP-like immunoreactivities did not overlap. These results indicate that the neuronal isoforms of the VGSC are mainly expressed in the AL and that the neuron-like cells in the ALs express VGSCs. Our findings indicate that AL neurons generate action potentials and send sensory information to the motor systems on the contralateral side of the spinal segment.

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“…Rosenberg and Necker (2002) found dendritic projections of the accessory lobe neurons that extend into fluidfilled lacunae, analogous to the stereocilia of inner ear hair cells. Cells in the accessory lobes have neuronal-type voltage-gated sodium channels (Yamanaka et al, 2008, Matsushita et al, 2018, indicating the presence of neurons that can generate action potentials and are thus capable of acting as Necker suggests. In addition, there is evidence that implicates GABA (Yamanaka et al, 2012), glutamate (Yamanaka et al, 2013), and acetylcholine (Takahashi et al, 2015) in accessory lobe neuron function.…”

Section: A Mechanosensory Function For the Lsomentioning

confidence: 99%

The balance hypothesis for the avian lumbosacral organ and an exploration of its morphological variation

Stanchak

French

Perkel

et al. 2020

Preprint

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Birds (Aves) exhibit exceptional and diverse locomotor behaviors, including the exquisite ability to balance on two feet. How birds so precisely control their movements may be partly explained by a set of intriguing modifications in their lower spine. These modifications are collectively known as the lumbosacral organ (LSO) and are found in the fused lumbosacral vertebrae called the synsacrum. They include a set of transverse canal-like recesses in the synsacrum that align with lateral lobes of the spinal cord, as well as a dorsal groove in the spinal cord that houses an egg-shaped glycogen body. Based on compelling but primarily observational data, the most recent functional hypotheses for the LSO consider it to be a secondary balance organ, in which the transverse canals are analogous to the semicircular canals of the inner ear. If correct, this hypothesis would reshape our understanding of avian locomotion, yet the LSO has been largely overlooked in the recent literature. Here, we review the current evidence for this hypothesis and then explore a possible relationship between the LSO and balance-intensive locomotor ecologies.Our comparative morphological dataset consists of micro-computed tomography (μ-CT) scans of synsacra from ecologically diverse species. We find that birds that perch tend to have more prominent transverse canals, suggesting that the LSO is useful for balance-intensive behaviors.We then identify the crucial outstanding questions about LSO structure and function. The LSO may be a key innovation that allows independent but coordinated motion of the head and the body, and a full understanding of its function and evolution will require multiple interdisciplinary research efforts. Jargon-FreeBirds have an uncanny ability to move their heads independently of their bodies. They can keep their heads remarkably still to focus on their prey while twisting in flight or perched on a bouncing branch. How are they able to do this? Like us, birds have balance organs in their inner ears that act like gyroscopes. Surprisingly, birds may have an additional balance organ known as the "lumbosacral organ" in their spine, right above their legs, which might help them sense the movement of their body separately from their head. This second balance organ may have played a very important role in bird evolution and how birds move, but it has seldom been considered in recent scientific studies. This intriguing hypothesis is based in part on a series of fluid-filled, canal-like recesses in the bone surrounding the spinal cord, which resemble the semicircular canals of the inner ear. We looked for evidence of these canal-like recesses in many different bird species, and we found it in every bird we examined. We also found that birds that perch often have deeper recesses than birds that do not perch, suggesting these canals help maintain balance. This paper presents those findings, reviews the existing research, and identifies some key questions that need to be asked to advance our understanding of this fascinating and ...

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Chick spinal accessory lobes contain functional neurons expressing voltagegated sodium channels generating action potentials

Cited by 11 publications

References 17 publications

A Physical Model Suggests That Hip-Localized Balance Sense in Birds Improves State Estimation in Perching: Implications for Bipedal Robots

A Physical Model Suggests That Hip-Localized Balance Sense in Birds Improves State Estimation in Perching: Implications for Bipedal Robots

<b>Neuron-like cells in the chick spinal accessory lobe express neuronal-type voltage-gated sodium </b><b>channels </b>

The balance hypothesis for the avian lumbosacral organ and an exploration of its morphological variation

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