Proprioceptor

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Thomas M Jessell - One of the best experts on this subject based on the ideXlab platform.

  • a role for sensory end organ derived signals in regulating muscle spindle Proprioceptor phenotype
    The Journal of Neuroscience, 2019
    Co-Authors: Dawei Wu, Ira Schieren, Yingzhi Qian, Thomas M Jessell, Chaolin Zhang, Joriene C De Nooij
    Abstract:

    Proprioceptive feedback from Group Ia/II muscle spindle afferents and Group Ib Golgi tendon afferents is critical for the normal execution of most motor tasks, yet how these distinct Proprioceptor subtypes emerge during development remains poorly understood. Using molecular genetic approaches in mice of either sex, we identified 24 transcripts that have not previously been associated with a Proprioceptor identity. Combinatorial expression analyses of these markers reveal at least three molecularly distinct Proprioceptor subtypes. In addition, we find that 12 of these transcripts are expressed well after Proprioceptors innervate their respective sensory receptors, and expression of three of these markers, including the heart development molecule Heg1 , is significantly reduced in mice that lack muscle spindles. These data reveal Heg1 as a putative marker for proprioceptive muscle spindle afferents. Moreover, they suggest that the phenotypic specialization of functionally distinct Proprioceptor subtypes depends, in part, on extrinsic sensory receptor organ-derived signals. SIGNIFICANCE STATEMENT Sensory feedback from muscle spindle (MS) and Golgi tendon organ (GTO) sensory end organs is critical for normal motor control, but how distinct MS and GTO afferent sensory neurons emerge during development remains poorly understood. Using (bulk) transcriptome analysis of genetically identified Proprioceptors, this work reveals molecular markers for distinct Proprioceptor subsets, including some that appear selectively expressed in MS afferents. Detailed analysis of the expression of these transcripts provides evidence that MS/GTO afferent subtype phenotypes may, at least in part, emerge through extrinsic, sensory end organ-derived signals.

  • A Role for Sensory end Organ-Derived Signals in Regulating Muscle Spindle Proprioceptor Phenotype.
    The Journal of neuroscience : the official journal of the Society for Neuroscience, 2019
    Co-Authors: Ira Schieren, Yingzhi Qian, Thomas M Jessell, Chaolin Zhang, Joriene C De Nooij
    Abstract:

    Proprioceptive feedback from group Ia/II muscle spindle afferents and group Ib Golgi tendon afferents is critical for the normal execution of most motor tasks, yet how these distinct Proprioceptor subtypes emerge during development remains poorly understood. Using molecular genetic approaches in mice of either sex, we identified twenty-four transcripts that have not previously been associated with a Proprioceptor identity. Combinatorial expression analyses of these markers reveal at least three molecularly distinct Proprioceptor subtypes. In addition, we find that twelve of these transcripts are expressed well after Proprioceptors innervate their respective sensory receptors, and expression of three of these markers — including the heart development molecule Heg1 - is significantly reduced in mice that lack muscle spindles. These data reveal Heg1 as a putative marker for proprioceptive muscle spindle afferents. Moreover, they suggest that the phenotypic specialization of functionally distinct Proprioceptor subtypes depends, in part, on extrinsic sensory receptor organ-derived signals. Significance statement: Sensory feedback from muscle spindle (MS) and Golgi tendon organ (GTO) sensory end-organs is critical for normal motor control, but how distinct MS and GTO afferent sensory neurons emerge during development remains poorly understood. Using (bulk) transcriptome analysis of genetically identified Proprioceptors, this work reveals molecular markers for distinct Proprioceptor subsets, including some that appear selectively expressed in MS afferents. Detailed analysis of the expression of these transcripts provides evidence that MS/GTO afferent subtype phenotypes may, at least in part, emerge through extrinsic - sensory end-organ derived - signals.

  • muscle type identity of Proprioceptors specified by spatially restricted signals from limb mesenchyme
    Cell, 2016
    Co-Authors: Sebastian Poliak, Thomas M Jessell, Amy Norovich, Masahito Yamagata, Joshua R Sanes
    Abstract:

    The selectivity with which proprioceptive sensory neurons innervate their central and peripheral targets implies that they exhibit distinctions in muscle-type identity. The molecular correlates of Proprioceptor identity and its origins remain largely unknown, however. In screens to define muscle-type Proprioceptor character, we find all-or-none differences in gene expression for Proprioceptors that control antagonistic muscles at a single hindlimb joint. Analysis of three of these genes, cadherin13 (cdh13), semaphorin5a (sema5a), and cartilage-acidic protein-1 (crtac1), reveals expression in Proprioceptor subsets that supply muscle groups located at restricted dorsoventral and proximodistal domains of the limb. Genetically altering the dorsoventral character of the limb mesenchyme elicits a change in the profile of Proprioceptor cdh13, sema5a, and crtac1 expression. These findings indicate that Proprioceptors acquire aspects of their muscle-type identity in response to mesenchymal signals expressed in restricted proximodistal and dorsoventral domains of the developing limb.

  • piezo2 is the principal mechanotransduction channel for proprioception
    Nature Neuroscience, 2015
    Co-Authors: Viktor Lukacs, Joriene C De Nooij, Thomas M Jessell, Dasha Zaytseva, Connor R Criddle, Allain G Francisco, Katherine A Wilkinson, Ardem Patapoutian
    Abstract:

    Proprioception, the sense of body and limb position, begins in nerve cells called Proprioceptors that are activated by muscle or joint stretch. The molecular mechanism of mechanotransduction in mammalian Proprioceptors is unknown. The authors show that the mechanically activated cation channel Piezo2 is the principal mechanotransducer in murine Proprioceptors.

  • piezo2 is the principal mechanotransduction channel for proprioception
    Nature Neuroscience, 2015
    Co-Authors: Seunghyun Woo, Joriene C De Nooij, Thomas M Jessell, Viktor Lukacs, Dasha Zaytseva, Connor R Criddle, Allain G Francisco, Katherine A Wilkinson, Ardem Patapoutian
    Abstract:

    Proprioception, the perception of body and limb position, is mediated by Proprioceptors, specialized mechanosensory neurons that convey information about the stretch and tension experienced by muscles, tendons, skin and joints. In mammals, the molecular identity of the stretch-sensitive channel that mediates proprioception is unknown. We found that the mechanically activated nonselective cation channel Piezo2 was expressed in sensory endings of Proprioceptors innervating muscle spindles and Golgi tendon organs in mice. Two independent mouse lines that lack Piezo2 in proprioceptive neurons showed severely uncoordinated body movements and abnormal limb positions. Moreover, the mechanosensitivity of parvalbumin-expressing neurons that predominantly mark Proprioceptors was dependent on Piezo2 expression in vitro, and the stretch-induced firing of Proprioceptors in muscle-nerve recordings was markedly reduced in Piezo2-deficient mice. Together, our results indicate that Piezo2 is the major mechanotransducer of mammalian Proprioceptors.

Joriene C De Nooij - One of the best experts on this subject based on the ideXlab platform.

  • molecular development of muscle spindle and golgi tendon organ sensory afferents revealed by single Proprioceptor transcriptome analysis
    bioRxiv, 2020
    Co-Authors: Katherine M Oliver, Danny M Florezpaz, Tudor C Badea, George Z Mentis, Vilas Menon, Joriene C De Nooij
    Abstract:

    Anatomical and physiological analyses have long revealed differences between proprioceptive groups Ia, II, and Ib sensory neurons, yet the molecular correlates of these three muscle afferent subtypes remain unknown. We performed single cell RNA sequencing of genetically identified adult Proprioceptors and, using unbiased bioinformatics approaches, detected five molecularly distinct neuronal clusters. Validation of cluster-specific transcripts in dorsal root ganglia (DRG) and skeletal muscle provides evidence these clusters correspond to functionally distinct muscle spindle (MS) or Golgi tendon organ (GTO) afferent Proprioceptors. Remarkably, while we uncovered just one type of GTO afferents, four of the five clusters represent MS afferents, thus demonstrating a previously unappreciated diversity among these muscle Proprioceptors. In vitro electrophysiological recordings reveal just two broadly distinct Proprioceptor types, and suggest that the refinement of functional subtype diversity may occur along multiple axes of maturation. Lineage analysis between Proprioceptor transcriptomes at different developmental stages show little or no correlation for transcripts that define adult MS or GTO afferents, supporting the idea that Proprioceptor subtype identity emerges late in development. Together, our data provide the first comprehensive molecular signature for groups Ia and II MS afferents and group Ib GTO afferents, and offer new strategies for genetic interrogation of the role of these individual Proprioceptor subtypes in regulating voluntary motor behavior.

  • a role for sensory end organ derived signals in regulating muscle spindle Proprioceptor phenotype
    The Journal of Neuroscience, 2019
    Co-Authors: Dawei Wu, Ira Schieren, Yingzhi Qian, Thomas M Jessell, Chaolin Zhang, Joriene C De Nooij
    Abstract:

    Proprioceptive feedback from Group Ia/II muscle spindle afferents and Group Ib Golgi tendon afferents is critical for the normal execution of most motor tasks, yet how these distinct Proprioceptor subtypes emerge during development remains poorly understood. Using molecular genetic approaches in mice of either sex, we identified 24 transcripts that have not previously been associated with a Proprioceptor identity. Combinatorial expression analyses of these markers reveal at least three molecularly distinct Proprioceptor subtypes. In addition, we find that 12 of these transcripts are expressed well after Proprioceptors innervate their respective sensory receptors, and expression of three of these markers, including the heart development molecule Heg1 , is significantly reduced in mice that lack muscle spindles. These data reveal Heg1 as a putative marker for proprioceptive muscle spindle afferents. Moreover, they suggest that the phenotypic specialization of functionally distinct Proprioceptor subtypes depends, in part, on extrinsic sensory receptor organ-derived signals. SIGNIFICANCE STATEMENT Sensory feedback from muscle spindle (MS) and Golgi tendon organ (GTO) sensory end organs is critical for normal motor control, but how distinct MS and GTO afferent sensory neurons emerge during development remains poorly understood. Using (bulk) transcriptome analysis of genetically identified Proprioceptors, this work reveals molecular markers for distinct Proprioceptor subsets, including some that appear selectively expressed in MS afferents. Detailed analysis of the expression of these transcripts provides evidence that MS/GTO afferent subtype phenotypes may, at least in part, emerge through extrinsic, sensory end organ-derived signals.

  • A Role for Sensory end Organ-Derived Signals in Regulating Muscle Spindle Proprioceptor Phenotype.
    The Journal of neuroscience : the official journal of the Society for Neuroscience, 2019
    Co-Authors: Ira Schieren, Yingzhi Qian, Thomas M Jessell, Chaolin Zhang, Joriene C De Nooij
    Abstract:

    Proprioceptive feedback from group Ia/II muscle spindle afferents and group Ib Golgi tendon afferents is critical for the normal execution of most motor tasks, yet how these distinct Proprioceptor subtypes emerge during development remains poorly understood. Using molecular genetic approaches in mice of either sex, we identified twenty-four transcripts that have not previously been associated with a Proprioceptor identity. Combinatorial expression analyses of these markers reveal at least three molecularly distinct Proprioceptor subtypes. In addition, we find that twelve of these transcripts are expressed well after Proprioceptors innervate their respective sensory receptors, and expression of three of these markers — including the heart development molecule Heg1 - is significantly reduced in mice that lack muscle spindles. These data reveal Heg1 as a putative marker for proprioceptive muscle spindle afferents. Moreover, they suggest that the phenotypic specialization of functionally distinct Proprioceptor subtypes depends, in part, on extrinsic sensory receptor organ-derived signals. Significance statement: Sensory feedback from muscle spindle (MS) and Golgi tendon organ (GTO) sensory end-organs is critical for normal motor control, but how distinct MS and GTO afferent sensory neurons emerge during development remains poorly understood. Using (bulk) transcriptome analysis of genetically identified Proprioceptors, this work reveals molecular markers for distinct Proprioceptor subsets, including some that appear selectively expressed in MS afferents. Detailed analysis of the expression of these transcripts provides evidence that MS/GTO afferent subtype phenotypes may, at least in part, emerge through extrinsic - sensory end-organ derived - signals.

  • piezo2 is the principal mechanotransduction channel for proprioception
    Nature Neuroscience, 2015
    Co-Authors: Viktor Lukacs, Joriene C De Nooij, Thomas M Jessell, Dasha Zaytseva, Connor R Criddle, Allain G Francisco, Katherine A Wilkinson, Ardem Patapoutian
    Abstract:

    Proprioception, the sense of body and limb position, begins in nerve cells called Proprioceptors that are activated by muscle or joint stretch. The molecular mechanism of mechanotransduction in mammalian Proprioceptors is unknown. The authors show that the mechanically activated cation channel Piezo2 is the principal mechanotransducer in murine Proprioceptors.

  • piezo2 is the principal mechanotransduction channel for proprioception
    Nature Neuroscience, 2015
    Co-Authors: Seunghyun Woo, Joriene C De Nooij, Thomas M Jessell, Viktor Lukacs, Dasha Zaytseva, Connor R Criddle, Allain G Francisco, Katherine A Wilkinson, Ardem Patapoutian
    Abstract:

    Proprioception, the perception of body and limb position, is mediated by Proprioceptors, specialized mechanosensory neurons that convey information about the stretch and tension experienced by muscles, tendons, skin and joints. In mammals, the molecular identity of the stretch-sensitive channel that mediates proprioception is unknown. We found that the mechanically activated nonselective cation channel Piezo2 was expressed in sensory endings of Proprioceptors innervating muscle spindles and Golgi tendon organs in mice. Two independent mouse lines that lack Piezo2 in proprioceptive neurons showed severely uncoordinated body movements and abnormal limb positions. Moreover, the mechanosensitivity of parvalbumin-expressing neurons that predominantly mark Proprioceptors was dependent on Piezo2 expression in vitro, and the stretch-induced firing of Proprioceptors in muscle-nerve recordings was markedly reduced in Piezo2-deficient mice. Together, our results indicate that Piezo2 is the major mechanotransducer of mammalian Proprioceptors.

Hiroyuki Ichikawa - One of the best experts on this subject based on the ideXlab platform.

  • Development of primary sensory neurons in the trigeminal nervous system; dependency on neurotrophins and other substances
    Elsevier, 2012
    Co-Authors: Hiroyuki Ichikawa, Saburo Matsuo, Tomosada Sugimoto
    Abstract:

    This review presents information about the development of primary sensory neurons in the trigeminal nervous system. The deficiency of high affinity receptors for nerve growth factor (trkA) and neurotrophin-3 (trk-C) causesa reduction of primary nociceptors in the trigeminal ganglion (TG). The disruption of trkB, a receptor for brain-derived neurotrophic factor and neurotrophin-4, causes a loss of Meissner endings in the palate and Ruffini endings in the periodontal ligament. The number of Merkel cells in palatal rugae is also severely reduced by the absence of trkA, trkB or trkC. In the mesencephalic trigeminal tract nucleus (Mes5), primary Proprioceptors are decreased by 50% in trkC null mutant mice. On the other hand, the deficiency of Brn-3a, a member of the POU family of transcription factors, decreases primary nociceptors and low-threshold mechanoreceptors in the TG. In the Mes5 of Brn-3a knockout mice, primary Proprioceptors are completely lost. In addition, the disruption of dystonin which is a member of the plakin family of high molecular weight cytoskeletal linker proteins causes a reduction of nociceptors in the TG but not Proprioceptors in the Mes5. The dependency of primary nociceptors, low-threshold mechanoreceptors and Proprioceptors on neurotrophins, Brn-3a and dystonin in the trigeminal nervous system is discussed

  • the reduction of Proprioceptors in the mesencephalic trigeminal tract nucleus after neonatal masseteric nerve transection effect of brain derived neurotrophic factor
    Brain Research, 2007
    Co-Authors: Hiroyuki Ichikawa, Saburo Matsuo, H W Jin, S Terayama, Tomoichiro Yamaai, Tomosada Sugimoto
    Abstract:

    Abstract The effect of neonatal masseteric nerve transection on primary Proprioceptors was examined in the mesencephalic trigeminal tract nucleus (Mes5) of the rat. At 72 h to 21 days after the injury, the number of Mes5 neurons decreased on the side ipsilateral to the transection. The means ± SD of percentage proportion of ipsilateral/contralateral neurons at 72 h and 21 days were 69.9 ± 7.5% and 58.2 ± 14.6%, respectively. The application of brain-derived neurotrophic factor to the proximal stump of the masseteric nerve delayed the loss of Mes5 neurons at 72 h after the injury; the mean numbers ± SD of ipsilateral and contralateral Mes5 neurons in injured animals with BDNF application was 553.6 ± 61.9 and 558.4 ± 55.3, respectively. Saline application had no effect on the injury-induced loss of Mes5 neurons; i.e., the mean numbers ± SD of ipsilateral and contralateral Mes5 neurons were 367.3 ± 72.5 and 543 ± 33.5, respectively. These findings indicate that trigeminal primary Proprioceptors are sensitive to the neonatal injury. The survival of Proprioceptors during early postnatal period is probably dependent upon brain-derived neurotrophic factor in the trigeminal nervous system.

  • brn 3a is required for the generation of Proprioceptors in the mesencephalic trigeminal tract nucleus
    Brain Research, 2005
    Co-Authors: Hiroyuki Ichikawa, Mengqing Xiang, F Qiu, T Sugimoto
    Abstract:

    The distribution of motor and proprioceptive neurons was investigated in the trigeminal nervous system of wild-type and Brn-3a knockout mice at embryonic day 18.5 and postnatal day 0. We found that the trigeminal motor nucleus (Mo5) contained abundant motoneurons in wild-type (mean number +/- SD per section = 128 +/- 22, range = 93-167) and knockout (mean number +/- SD per section = 121 +/- 23, range = 75-158) mice and that the cell size of Mo5 neurons was similar between these mice (wild-type, mean +/- SD = 165 +/- 59 microm2, range = 65-326 microm2; knockout, mean +/- SD = 167 +/- 59 microm2, range = 71-327 microm2). Mo5 neurons were immunoreactive for calcitonin gene-related peptide and such immunoreactive neurons were abundant in both wild-type and mutant mice. In the mesencephalic tract nucleus (Mes5) of wild-type mice, many Proprioceptors (mean number +/- SD per section = 56 +/- 19, range = 27-85) that contained parvalbumin immunoreactivity were also observed. In knockout mice, however, Mes5 neurons could not be detected. The area of brainstems which normally contained the Mes5 was devoid of parvalbumin-immunoreactive Proprioceptors. The present study suggests that Brn-3a is required for the development of Proprioceptors but not motoneurons in the trigeminal nervous system.

  • effect of brn 3a deficiency on parvalbumin immunoreactive primary sensory neurons in the dorsal root ganglion
    Developmental Brain Research, 2004
    Co-Authors: Hiroyuki Ichikawa, Mengqing Xiang, Tomosada Sugimoto
    Abstract:

    Immunohistochemistry for parvalbumin, a marker for primary Proprioceptors, was performed on the dorsal root ganglion (DRG) of wildtype and knockout mice for Brn-3a at postnatal day 0 and embryonic day 18.5. The DRG contained many parvalbumin-immunoreactive (ir) neurons in wildtype (5.4%) and knockout mice (5.6%). Cell size analysis demonstrated that such neurons were mostly medium-sized to large in these mice. Therefore, it is unlikely that the survival of Proprioceptors is dependent upon Brn-3a in the DRG. In the dorsal column and gray matter of the spinal cord of knockout mice, however, parvalbumin-ir nerve fibers were sparse compared to wildtype mice. The number of parvalbumin-ir varicosities around motoneurons decreased in the mutant. Thus, our data suggest that Brn-3a may play an important role in the central projection and terminal formation of DRG Proprioceptors in the spinal cord.

Tomosada Sugimoto - One of the best experts on this subject based on the ideXlab platform.

  • Development of primary sensory neurons in the trigeminal nervous system; dependency on neurotrophins and other substances
    Elsevier, 2012
    Co-Authors: Hiroyuki Ichikawa, Saburo Matsuo, Tomosada Sugimoto
    Abstract:

    This review presents information about the development of primary sensory neurons in the trigeminal nervous system. The deficiency of high affinity receptors for nerve growth factor (trkA) and neurotrophin-3 (trk-C) causesa reduction of primary nociceptors in the trigeminal ganglion (TG). The disruption of trkB, a receptor for brain-derived neurotrophic factor and neurotrophin-4, causes a loss of Meissner endings in the palate and Ruffini endings in the periodontal ligament. The number of Merkel cells in palatal rugae is also severely reduced by the absence of trkA, trkB or trkC. In the mesencephalic trigeminal tract nucleus (Mes5), primary Proprioceptors are decreased by 50% in trkC null mutant mice. On the other hand, the deficiency of Brn-3a, a member of the POU family of transcription factors, decreases primary nociceptors and low-threshold mechanoreceptors in the TG. In the Mes5 of Brn-3a knockout mice, primary Proprioceptors are completely lost. In addition, the disruption of dystonin which is a member of the plakin family of high molecular weight cytoskeletal linker proteins causes a reduction of nociceptors in the TG but not Proprioceptors in the Mes5. The dependency of primary nociceptors, low-threshold mechanoreceptors and Proprioceptors on neurotrophins, Brn-3a and dystonin in the trigeminal nervous system is discussed

  • the reduction of Proprioceptors in the mesencephalic trigeminal tract nucleus after neonatal masseteric nerve transection effect of brain derived neurotrophic factor
    Brain Research, 2007
    Co-Authors: Hiroyuki Ichikawa, Saburo Matsuo, H W Jin, S Terayama, Tomoichiro Yamaai, Tomosada Sugimoto
    Abstract:

    Abstract The effect of neonatal masseteric nerve transection on primary Proprioceptors was examined in the mesencephalic trigeminal tract nucleus (Mes5) of the rat. At 72 h to 21 days after the injury, the number of Mes5 neurons decreased on the side ipsilateral to the transection. The means ± SD of percentage proportion of ipsilateral/contralateral neurons at 72 h and 21 days were 69.9 ± 7.5% and 58.2 ± 14.6%, respectively. The application of brain-derived neurotrophic factor to the proximal stump of the masseteric nerve delayed the loss of Mes5 neurons at 72 h after the injury; the mean numbers ± SD of ipsilateral and contralateral Mes5 neurons in injured animals with BDNF application was 553.6 ± 61.9 and 558.4 ± 55.3, respectively. Saline application had no effect on the injury-induced loss of Mes5 neurons; i.e., the mean numbers ± SD of ipsilateral and contralateral Mes5 neurons were 367.3 ± 72.5 and 543 ± 33.5, respectively. These findings indicate that trigeminal primary Proprioceptors are sensitive to the neonatal injury. The survival of Proprioceptors during early postnatal period is probably dependent upon brain-derived neurotrophic factor in the trigeminal nervous system.

  • effect of brn 3a deficiency on parvalbumin immunoreactive primary sensory neurons in the dorsal root ganglion
    Developmental Brain Research, 2004
    Co-Authors: Hiroyuki Ichikawa, Mengqing Xiang, Tomosada Sugimoto
    Abstract:

    Immunohistochemistry for parvalbumin, a marker for primary Proprioceptors, was performed on the dorsal root ganglion (DRG) of wildtype and knockout mice for Brn-3a at postnatal day 0 and embryonic day 18.5. The DRG contained many parvalbumin-immunoreactive (ir) neurons in wildtype (5.4%) and knockout mice (5.6%). Cell size analysis demonstrated that such neurons were mostly medium-sized to large in these mice. Therefore, it is unlikely that the survival of Proprioceptors is dependent upon Brn-3a in the DRG. In the dorsal column and gray matter of the spinal cord of knockout mice, however, parvalbumin-ir nerve fibers were sparse compared to wildtype mice. The number of parvalbumin-ir varicosities around motoneurons decreased in the mutant. Thus, our data suggest that Brn-3a may play an important role in the central projection and terminal formation of DRG Proprioceptors in the spinal cord.

Anthony Newman Taylor - One of the best experts on this subject based on the ideXlab platform.

  • Give Proprioceptors a chance.
    Advances in experimental medicine and biology, 2002
    Co-Authors: Anthony Newman Taylor
    Abstract:

    The theme of this review is that it is inappropriate to regard Proprioceptors as general purpose transducers of system variables associated with movements. We should not try to describe their properties by general expressions derived by testing with a wide range of externally applied disturbances, in the way that is customary in engineering practice. Instead, if study is concentrated on their behaviour during natural active movements such as locomotion, then the significance of the signals which they feed back to the CNS is much easier to understand. This idea is developed briefly for tendon organs, and then in more detail for muscle spindles in locomotion.