Changes of c-Fos expression and NADPH-d activity in claustrum induced by chronic muscle inflammation in cat (a preliminary study)

Keywords: muscle inflammation, complete Freund’s adjuvant, claustrum, putamen, cat

Abstract

An investigation of the central mechanisms underlying muscle inflammation and musculoskeletal pain is an important step to find means for the prevention or treatment of muscle inflammation. One of the insufficiently studied brain structures involved in the transmission of nociceptive information is the claustrum (CL). Therefore, the aim of the study was to reveal changes in the patterns of Fos-immunoreactivity and NADPH-diaphoreactivity in the nucleus claustrum (CL) and additionally in the ventral putamen (Pu) during chronic inflammation of m. gastrocnemius-soleus in cat, induced by intramuscular injection of complete Freund’s adjuvant (CFA). Immunohistochemical and histochemical techniques were used to detect Fos-immunoreactive (Fos-ir) and NADPH-diaphorase reactive (NADPH-dr) neurons within studied structures. It was revealed that nine days after CFA-induced muscle inflammation the level of Fos-immunoreactivity and NADPH-d reactivity within the CL and in the ventral part of Pu increased two-fold in comparison with the control. Because the CL is reciprocally connected with many structures of the brain cortex and subcortical structures, all these structures can be pathways of transmission of nociceptive information, nevertheless, it can be assume that the central amygdala nucleus may make the main nociceptive contribution to the activation of neurons within the CL. It is known that CL is mutually related to Pu, but it was not possible to assess their mutual influence in this study. The results of the study of the Fos-ir neurons distribution in CL and Pu under conditions of long-term muscles inflammation indicate the active involvement of the mentioned structures in the formation of adaptive reactions. The increase in the number of neurons with NADPH-d reactivity in CL and Pu indicates that NO-signals play a significant role in the formation and amplification of the response to painful impulses from inflamed muscles. In addition, further research is needed to accurately identify all possible nociceptive inputs to the CL and to separate the emotional, motor, auditory, and visual components that may accompany nociceptive processes.

Downloads

Download data is not yet available.

References

Abbadie, C., & Besson, J. M. (1992). c-fos expression in rat lumbar spinal cord during the development of adjuvant-induced arthritis. Neuroscience, (48), 985-993. doi: 10.1016/0306-4522(92)90287-c

Baumgartner, U., Buchholz, H. G., Bellosevich, A., Magerl, W., Siessmeier, T., Rolke, R., & Schreckenberger, M. (2006). High opiate receptor binding potential in the human lateral pain system. Neuroimage, 30(3), 692-699. doi: 10.1016/j.neuroimage.2005.10.033

Braz, J. M., Nassar, M. A., Wood, J. N., & Basbaum, A. I. (2005). Parallel “pain” pathways arise from subpopulations of primary afferent nociceptor. Neuron, 47(6), 787-793. doi: 10.1016/j.neuron.2005.08.015

Crick, F. C., & Koch, C. (2005). What is the function of the claustrum? Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1458), 1271-1279. doi: 10.1098/rstb.2005.1661

Darques, J. L., & Jammes, Y. (1997). Fatigue-induced changes in group IV muscle afferent activity: differences between high- and low-frequency electrically induced fatigues. Brain Research, 750(1-2), 147-154. doi: 10.1016/s0006-8993(96)01341-8

Gad, M. Z., & Khattab, M. (2000). Modulation of nitric oxide synthesis in inflammation. Relationship to oxygen-derived free radicals and prostaglandin synthesis. Arzneimittelforschung, 50(5), 449-455. doi: 10.1055/s-0031-1300229

Garthwaite, J., & Boulton, C. L. (1995). Nitric oxide signaling in the central nervous system. Annual Review of Physiology, (57), 683-706.

Giesler, G. J., Katter, J. T., & Dado, R. J. (1994). Direct spinal pathways to the limbic system for nociceptive information. Trends in Neurosciences, 17(6), 244-250. doi: 10.1016/0166-2236(94)90007-8

Govsa, F., Kayalioglu, G., Erdem, B. Maisky, V. A., & Hariri, N. (1998). Laminar distribution of the sources of ascending spino-supraspinal pathways involved in nociceptive transmission and pain modulation. Turkish Journal of Medical Sciences, 28(1), 41-46.

Gracely, R. H., Geisser, M. E., Giesecke, T. B., Grant, M. A., Petzke, F., Williams, D. A., & Clauw, D. J. (2004). Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain, 127(4), 835-843. doi: 10.1093/brain/awh098

Guirado, S., Real, M. Á., Olmos, J. L., & Dávila, J. C. (2003). Distinct types of nitric oxide-producing neurons in the developing and adult mouse claustrum. Journal of Comparative Neurology, 465(3), 431-444. doi: 10.1002/cne.10835

Harris, J. A. (1998). Using c-fos as a neural marker of pain. Brain Research Bulletin, 45(1), 1-8. doi: 10.1016/s0361-9230(97)00277-3

Hinova-Palova, D. V., Paloff, A., Christova, T., & Ovtscharoff, W. (1997). Topographical distribution of NADPH-diaphorase-positive neurons in the cat’s claustrum. European Journal of Morphology, 35(2), 105-116. doi: 10.1076/ejom.35.2.105.13068

Holscher, C. (1997). Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends in Neurosciences, (57), 683-706. doi: 10.1146/annurev.ph.57.030195.003343

Hoque, K. E., Indorkar, R. P., Sammut, S., & West, A. R. (2010). Impact of dopamine-glutamate interactions on striatal neuronal nitric oxide synthase activity. Psychopharmacology, 207(4), 571-581. doi: 10.1007/s00213-009-1687-0

Hsu, S.-M., Raine, L., & Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. Journal of Histochemistry & Cytochemistry, 29(4), 577-580. doi: 10.1177/29.4.6166661

Kapakin, S. (2011). The claustrum: three-dimensional reconstruction, photorealistic imaging, and stereotactic approach. Folia morphologica, 70(4), 228–234.

Khalsa, P. S. (2004). Biomechanics of musculoskeletal pain: dynamics of the neuromatrix, Journal of Electromyography and Kinesiology, 14(1), 109-120. doi: 10.1016/j.jelekin.2003.09.020

Man’kovskaya, Y. P., Vlasenko, O. V., & Suprunov, K. V. (2012). Expression of c-Fos Protein and Activity of NO Synthase in the Mesolimbic Dopaminergic Structures and Dorsolateral Striatum of Rats Realizing Operant Food-Procuring Reflexes. Neurophysiology, 44(6), 433-440.

Mense, S. (1993). Nociception from skeletal muscle in relation to clinical muscle pain. Pain, (54), 241-289. doi: 10.1016/0304-3959(93)90027-M

Mikula, S., Trotts, I., Stone, J., & Jones, E. G. (2007). Internet-Enabled High-Resolution Brain Mapping and Virtual Microscopy. Neuroimage, 35(1), 9-15. doi: 10.1016/j.neuroimage.2006.11.053

Neugebauer, V., & Li, W. (2002). Processing of nociceptive mechanical and thermal information in central amygdala neurons with knee-joint input. Journal of Neurophysiology, 87(1), 103-112. doi: 10.1152/jn.00264.2001

Perrin-Terrin, An-S., Jeton, F., Pichon, A., Frugière, A., Richalet, Jean-P., Bodineau, L., & Voituron, N. (2016). The c-Fos protein immunohistological detection: A useful tool as a marker of central pathways involved in specific physiological responses in vivo and ex vivo. Journal of Visualized Experiments, 110(e), 53613. doi: 10.3791/53613

Raghavendra, V., Tanga, F. Y., & DeLeo, J. A. (2004). Complete Freunds adjuvant‐induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. European Journal of Neuroscience, 20(2), 467-473. doi: 10.1111/j.1460-9568.2004.03514.x

Schmid, H. A., & Pehl, U. (1996). Regional specific effects of nitric oxide donors and cGMP on the electrical activity of neurons in the rat spinal cord. Journal of Chemical Neuroanatomy, 10(3-4), 197-201. doi: 10.1016/0891-0618(96)00143-3

Sherk, H. (1986). The claustrum and the cerebral cortex. In: Cerebral Cortex. Sensory-Motor Areas and Aspects of Cortical Connectivity, edited by E. G. Jones and A. Peters, (5), 467-499.

Shima, K., Hoshi, E., & Tanji, J. (1996). Neuronal activity in the claustrum of the monkey during performance of multiple movements. Journal of Neurophysiology, 76(3), 2115-2119. doi: 10.1152/jn.1996.76.3.2115

Spike, R. C., Todd, A. J., & Johnston, H. M. (1993). Coexistence of NADPH-diaphorase with GABA, glycine, and acetylcholine in rat spinal cord. Journal of Comparative Neurology, 335(3), 320–333. doi: 10.1002/cne.903350303

Starr, C. J., Sawaki, L., Wittenberg, G. F., Burdette, J. H., Oshiro, Y., Quevedo, A. S. … Coghill, R. C. (2011). The contribution of the putamen to sensory aspects of pain: insights from structural connectivity and brain lesions. Brain, 134(7), 1987–2004. doi: 10.1093/brain/awr117

Steffens, H., Schomburg, E. D., Maznychenko, A. V., Maisky, V. A., Kostyukov, A. I., & Pilyavskii, A. I. (2007). Monosynaptic reflexes, c-fos expression, and NADPH-Diaphorase Activity in the cat spinal cord: changes induced by chronic muscle inflammation. Neurophysiology, 39(3), 191-200.

Vereshchaka, I. V., Bulgakova, N. V., Maznychenko, A. V., Gonchar, O. O., Prylutskyy, Y. I., Ritter, U., & Kostyukov, A. I. (2018). C60 fullerenes diminish muscle fatigue in rats comparable to N-acetylcysteine or beta-Alanine. Frontiers in Physiology, 9(12). doi: 10.3389/fphys.2018.00517

Vincent, S. R., & Kimura, H. (1992). Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience, 46(4), 755-784. doi: 10.1016/0306-4522(92)90184-4

Wei, F., Dubner, R., & Ren, K. (1999). Dorsolateral funiculus-lesions unmask inhibitory or disfacilitatory mechanisms which modulate the effects of innoxious mechanical stimulation on spinal Fos expression after inflammation. Brain Research, (820), 112-116. doi: 10.1016/s0006-8993(98)01359-6

Published
2022-12-24
How to Cite
Maznychenko, A. V., Abramovych, T. I., & Sokolowska, I. V. (2022). Changes of c-Fos expression and NADPH-d activity in claustrum induced by chronic muscle inflammation in cat (a preliminary study). Reports of Morphology, 28(4), 64-69. https://doi.org/10.31393/morphology-journal-2022-28(4)-09