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• W3180294623 abstract "We are grateful for the opportunity given to respond to Drs M. Hanani and R. Banks's Letter (Hanani & Banks, 2021) regarding our recent publication (Murase et al., 2021) in The Journal of Physiology. We have summarized the main comments (numbered as in the letter), each followed by our response. (1) Drs Hanani & Banks (2021) questioned whether the number of neurons innervating gastrocnemius muscle is too many when compared with that reported by Peyronnard et al. (1986). The number of dorsal root ganglion (DRG) neurons retrogradely traced differs with the method of dye application and the dye used. Peyronnard et al. (1986) used horseradish peroxidase (HRP) alone for a tracer to the cut end of the nerve, and it is known that uptake of HRP by nerve fibres is not good and HRP is broken down in the cell body (Kumar, 2019). In a later report (Swett et al. 1991), HRP, wheat germ agglutinin-conjugated HRP (WGA-HRP), or a mixture of both was used and it was reported that HRP tended to label more small neurons and WGA-HRP to label more large neurons, and therefore a mixture of both was used in Swett et al.’s paper. They reported a little larger number of neurons, 101–145, for medial gastrocnemius (GM), and 341 ± 60 for lateral gastrocnemius (GL) + soleus. In addition, Welin et al. (2008) reported 215 ± 8.1 GM neurons applying Fast Blue for 2 h to GM nerve, an about 2 times higher number of GM neurons than that reported by Peyronnard et al. Peyronnard et al. (1986) also counted fibre number in the GM-innervating nerve, and about 2.8 times more fibres than labelled GM DRG neurons were found. This ratio was calculated based on the assumption that all GM DRG were labelled by HRP, but this is not assured, as described above. If a ratio of 2.3 (reported by Langford and Coggeshall, 1981; proximal peripheral nerve vs. all DRG neurons) is employed, then the number of GM DRG neurons can be calculated to be 190, 2 times more than directly counted in DRGs (∼100), and near to the number reported by Welin et al. (2008). If the number of GL-innervating DRG neurons is more than that for GM, then the total number of DRG neurons innervating both GM and GL muscles might be around 500. Even if these are taken into consideration, the percentage of DRG neurons labelled in our paper might be high. We used Fluoro-Gold injected into both GL and GM muscles, and the number of injection sites was altogether 20, and 11 days elapsed until perfusion–fixation of the animal, so that as many DRG neurons innervating gastrocnemius muscle as possible were labelled. Fluoro-Gold is known not to leak from the labelled neurons in DRGs and to remain there for a long time (∼4 weeks: Novikova et al. 1997; Choi et al. 2002; Kumar, 2019). We took care not to leak dye to other muscles and the skin on injection, but there might have been some leakage to soleus, biceps femoris (which covers a large part of GL in rats) and other muscles of the backside of the lower hindlimb. Since the gastrocnemius muscle is largely covered with other muscles (e.g. biceps femoris) in rats, leakage to the skin must have been quite limited. If any, since the skin covering the backside of the lower hindlimb is mainly innervated by L5 (Takahashi et al. 1994), contamination must have been limited to L5. In addition, we are sure that leakage to the general circulation did not occur because no labelling was observed in S1 DRG (n = 2 rats). In conclusion, although the number of neurons labelled in our present study was larger than those in previous reports, we believe the majority of labelled neurons innervate the muscle. We should have cautiously discussed this point in the paper. (2.1) Drs Hanani and Banks pointed out that phosphorylated extracellular signal-regulated kinase (pERK) may be upregulated in satellite glias and this may contribute to hyperalgesia observed in our recent paper (Murase et al. 2021). As Drs Hanani and Banks pointed out, we also realized that satellite glias were stained with pERK, often strongly. This staining was observed not only in cases in which the mixture of low (0.1 μM) nerve growth factor (NGF) and low (0.008 μM) glial cell line-derived neurotrophic factor (GDNF) (which showed hyperalgesia) was injected but also in phosphate-buffered saline, low NGF and low GDNF groups (which showed no hyperalgesia). We could not find any tendency for pERK in satellite glias to be increased or decreased by the mixture of a low dose of NGF and GDNF. The role of satellite glias in hyperalgesia has been studied in inflammation models and nerve injury models, and in these models many mediators are involved. In our experiment we used only NGF and GDNF. So far we have not been able to find any reports that showed NGF or GDNF alone stimulates satellite glia. Although we could not find any tendency for pERK to increase in satellite glia, the satellite glia may contribute to hyperalgesia as Drs Hanani and Banks pointed out, and we should have touched on this point in the Discussion in our paper. (2.2) Drs Hanani and Banks also pointed out a discrepancy between the size of pERK positive gastrocnemius afferent neurons and that of the most muscle afferents. The size of pERK positive DRG neurons shown in Fig. 2A of our paper looks small. However, large to medium sized DRG neurons with pERK immunoreactivity did exist. We found that 4.8% of pERK positive neurons on administration of the mixture of low NGF (0.1 μM) and low GDNF (0.008 μM) to be of large size (>40 µm in diameter, that is >1200 µm2 in area), and 6.8% to be medium size (>30 µm in diameter, that is > 600 µm2 in area). There are many large TrkA+/GFRα1+ muscle DRG neurons, but not all of them contribute to nociception; rather, the majority of large neurons are considered to contribute to proprioception. As discussed in our paper: ‘Muscle nociception is believed to be mediated by thin-fibre afferents, namely unmyelinated (group IV) and thinly myelinated (group III) fibres (Kumazawa & Mizumura, 1977; Graven-Nielsen & Mense, 2001), and they are supposed to have small to medium-sized cell bodies. In addition, Lee et al. (1986) identified DRG neurons by intracellular recording and by intracellular dye injection, and found that there were cell bodies with unmyelinated axons that have diameters of 30 µm (corresponding to a cell area of 706 µm2)−49.9 µm (corresponding to a cell area of 1960 µm2), though in the cat. Similarly, Hoheisel & Mense (1987) recorded DRG neurons with unmyelinated axons that had cell areas >1200 µm2, i.e. were large neurons, in the cat. In the rat, neuronal size must be a little smaller in general than in cat.’ But there should be larger neurons with unmyelinated axons in the rat, too. The exact percentage of larger DRG neurons with thinly myelinated and unmyelinated axons is not known, but it may not be high. (3) Drs Hanani and Banks kindly pointed out other interaction mechanisms such as Devor & Wall (1990) reported. Drs Hanani and Banks suggested that satellite glial cells (SGCs) may mediate communications between different neurons via chemical messengers and gap junctions. We wonder whether the mutual cross talk in DRG neurons suggested in a paper by Devor & Wall (1990) occurs in response to NGF or GDNF or their mixture as commented by Drs Hanani and Banks. In Devor and Wall's paper, ‘crossed DRG excitation’ occurred in spontaneously active Aδ-axons but not C-axons. As we wrote in the citation in the response to comment 2.2, muscle nociception is usually mediated by thin fibres (Aδ- and C-fibres). In our previous studies, the ratio of muscular thin fibres with spontaneous activity was low (0∼50% in C-fibres, 0% in Aδ fibres) and discharge rate was in general low (≤0.1 imp/s) recorded in vitro (Taguchi et al. 2005; Murase et al. 2010, 2014). Intramuscular injection of NGF (high concentration, 0.8 µm, 5 µl) induced weak activation in only 20% of muscle thin-fibres (mainly C-fibres) (Murase et al. 2010), and that of GDNF (high concentration, 0.03 µm, 5 µl) induced excitation in 7/30 C-fibres and 2/14 Aδ-fibres with low discharge rate for a short time (Murase et al. 2014). Therefore, it is unlikely that cross-excitation in DRG was induced by the mixture of low NGF or low GDNF (concentration was 0.1 and 0.008 µm, respectively) used in our present paper. In addition, communication between different neurons mediated by SGCs might also be an interesting possibility, but we did not do any experiments addressing this point. When we try to take this experiment further, we will keep this idea in mind. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. No competing interests declared. All authors have read and approved the final version of this manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. Japan Society for the Promotion of Science (JSPS): K.M., JP23390154; Japan Society for the Promotion of Science (JSPS): T.T., JP20790191." @default.
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• W3180294623 date "2021-08-12" @default.
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• W3180294623 title "Reply from Shiori Murase, Kimiko Kobayashi, Teruaki Nasu, Chiaki Kihara, Toru Taguchi and Kazue Mizumura" @default.
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