Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic‐like vesicles: evidence from the rat muscle spindle primary sensory ending

Bewick, Guy S.; Reid, Brian; Richardson, Christine; Banks, Robert W.

doi:10.1113/jphysiol.2004.074799

Cited by 88 publications

(182 citation statements)

References 47 publications

(53 reference statements)

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“…Glutamate release can be induced in the periphery following stimulation of A or C sensory afferents (deGroot et al, 2000), and glutamate release from synaptic vesicles has been observed following stretch activation of mechanosensory nerve terminals innervating muscle spindles (Banks et al, 2002;Bewick et al, 2005). Our results strongly suggest that glutamate is crucial for maintaining the sensory capability of the piloneural collar.…”

Section: Discussionmentioning

confidence: 50%

Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor

et al. 2012

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SUMMARYThe piloneural collar in mammalian hairy skin comprises an intricate pattern of circumferential and longitudinal sensory afferents that innervate primary and secondary pelage hairs. The longitudinal afferents tightly associate with terminal Schwann cell processes to form encapsulated lanceolate nerve endings of rapidly adapting mechanoreceptors. The molecular basis for piloneural development, maintenance and function is poorly understood. Here, we show that Nefh-expressing glutamatergic neurons represent a major population of longitudinal and circumferential sensory afferents innervating the piloneural collar. Our findings using a VGLUT2 conditional-null mouse model indicate that glutamate is essential for innervation, patterning and differentiation of NMDAR + terminal Schwann cells during piloneural collar development. Similarly, treatment of adult mice with a selective NMDAR antagonist severely perturbed piloneural collar structure and reduced excitability of these mechanosensory neurons. Collectively, these results show that DRG-derived glutamate is essential for the proper development, maintenance and sensory function of the piloneural mechanoreceptor.

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Section: Discussionmentioning

confidence: 50%

Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor

et al. 2012

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“…However, it is uncertain whether glutamate may be released from the periodontal Ruffini endings and function as a neurotransmitter because glutamate is the most abundant excitatory neurotransmitter in the central nervous system. In the muscle spindles, Bewick et al (2005) proposed that glutamate release has an autogenic effect on excitability of the sensory endings. Thus, similar to the muscle spindle, we speculated that periodontal Ruffini endings released glutamate from axon terminals and this might contribute to the excitability of the endings.…”

Section: Vglut In Ruffini Endingsmentioning

confidence: 99%

Vesicular Glutamate Transporter Immunoreactivity in the Periodontal Ligament of the Rat Incisor

Honma

Kato

Shi

et al. 2011

The Anatomical Record

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The distribution of three vesicular glutamate transporter (VGluT) isoforms, VGluT1, VGluT2, and VGluT3, were investigated in the trigeminal ganglion of the periodontal ligament in the rat incisor-a receptive field of trigeminal ganglion neurons. In the trigeminal ganglion, mRNAs for all VGluT isoforms were detected and proteins were observed in the cytoplasm of trigeminal ganglion cells. VGluT1 immunoreactions were localized within the cytoplasm for all sizes of trigeminal neurons, although predominately in medium-large trigeminal neurons. Doublelabeling showed that most VGluT1 contained both VGluT2 and VGluT3. In the periodontal ligament of the incisor, the Ruffini endings, principal periodontal mechanoreceptors, displayed VGluT1 and VGluT2 immunoreactivities. However, lacked immunoreactions for VGluT3. At the electron microscopic level, VGluT1 immunoreactions were localized around the vesicle membranes at the axon terminal of Ruffini endings. The present results indicate that VGluT is expressed in the sensory nerve endings where apparent synapses are not present. Thus, glutamate in the sensory nerve endings is thought to be used in metabotropic functions. This is because glutamate is a general metabolic substrate, and/or acts as a neurotransmitter as proposed in muscle spindles. Anat Rec, 295:160-166, 2012. V V C 2011 Wiley Periodicals, Inc.

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“…The dyes then label intracellular membranes, and this labeling is irreversible. However, in hair cells that are not mechanically stimulated 13,14 and in fully differentiated primary sensory nerve terminals in situ, such as Ia endings in muscle spindles 15 , and in the lanceolate endings here 7 , styryl dye labeling seems to reflect membrane endocytosis, since labeling is reversible and does not block the mechanosensory responses 7,15,16 . While some dye internalization by channel permeation in these endings cannot be ruled out completely, it is clear from the continued firing during dye incubation and the reversibility of the labeling that the great majority of the labeling in differentiated terminals in situ is by internalization with recycling vesicle membrane.…”

Section: Discussionmentioning

confidence: 99%

Combined Recording of Mechanically Stimulated Afferent Output and Nerve Terminal Labelling in Mouse Hair Follicle Lanceolate Endings

Bewick

Cahusac

Banks

2016

JoVE

Self Cite

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A novel dissection and recording technique is described for monitoring afferent firing evoked by mechanical displacement of hairs in the mouse pinna. The technique is very cost-effective and easily undertaken with materials commonly found in most electrophysiology laboratories, or easily purchased. The dissection is simple and fast, with the mechanical displacement provided by a generic electroceramic wafer controlled by proprietary software. The same software also records and analyses the electroneurogram output. The recording of the evoked nerve activity is through a commercial differential amplifier connected to fire-polished standard glass microelectrodes. Helpful tips are given for improving the quality of the preparation, the stimulation and the recording conditions to optimize recording quality. The system is suitable for assaying the electrophysiological and optical properties of lanceolate terminals of palisade endings of hair follicles, as well as the outcomes from their pharmacological and/or genetic manipulation. An example of combining electrical recording with mechanical stimulation and labeling with a styryl pyridinium vital dye is given.

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Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic‐like vesicles: evidence from the rat muscle spindle primary sensory ending

Cited by 88 publications

References 47 publications

Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor

Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor

Vesicular Glutamate Transporter Immunoreactivity in the Periodontal Ligament of the Rat Incisor

Combined Recording of Mechanically Stimulated Afferent Output and Nerve Terminal Labelling in Mouse Hair Follicle Lanceolate Endings

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