Biology:Femoral chordotonal organ

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Short description: Sensory organ in insect legs
Figure 1. The femoral chordotonal organ in the femur of the fruit fly. Left: A picture of the cells of femoral chordotonal organ (labeled with green fluorescent protein) in the femur of the fruit fly. Right: A drawing of a fruit fly showing the location of the femur and the tibia. The femoral chordotonal organ senses the movements and the position of the femur-tibia joint.

The femoral chordotonal organ is a group of mechanosensory neurons found in an insect leg (Figure 1) that detects the movements and the position of the femur/tibia joint.[1] It is thought to function as a proprioceptor that is critical for precise control of leg position by sending the information regarding the femur/tibia joint to the motor circuits in the ventral nerve cord and the brain[2][3][4][5]

Structure

The cell bodies of the femoral chordotonal neurons are generally located in the proximal femur,[1] and their dendrites are mechanically coupled to the tibia through different types of tendons.[6][7][8][9][10] In Drosophila, where it is possible to genetically identify different subtypes of femoral chordotonal neurons, the neurons can be divided into three subtypes based on their axonal projection pattern into the ventral nerve cord[11] (Figure 2). The axons of the club neurons project to the center of the ventral nerve cord and form a bundle that is shaped like a club.[12] The axons of the claw neurons split into three branches that are shaped like a claw.[12] The axons of the hook neurons are shaped similar to the peavey hook.[11]

Sensory coding

Figure 2. Functional subtypes of femoral chordotonal neurons in the fruit fly. Left: A drawing of a fruit fly showing the location of the ventral nerve cord, where the axons of the femoral chordotonal neurons project to. Center: A drawing of the axon projection pattern of the different subtypes of femoral chordotonal neurons in the fruit fly. Right: Kinematic features of the femur-tibia joint encoded by different subtypes of femoral chordotonal neurons.

The sensory neurons of the femoral chordotonal organ encode various kinematic features of the femur/tibia joint including, position, speed, acceleration, and vibration.[13][14][15][16][17][18][19] In Drosophila, where it is possible to genetically track different subtypes of femoral chordotonal neurons, it is known that these different kinematic features are encoded by anatomically distinct subtypes of neurons mentioned above[11] (Figure 2). The position of the tibia is encoded by the claw neurons, vibrations are encoded by the club neurons, and the direction of the movement is encoded by the hook neurons.[11]

Function

The femoral chordotonal organ is thought to be involved in precise control of leg movements, and the experimental manipulations of the femoral chordotonal organ in stick insects and locusts have shown that they play a critical role during walking.[2] and target reaching[3]

Figure 3. A reflex involving the femoral chordotonal organ changes based on the behavioral state of the animal. Left-Top: During standing, flexion of the tibia detected by the femoral chordotonal organ activates a reflex that resists the movement and stabilize the posture. Left-Bottom: During walking, the same flexion of the tibia leads to an assistive reflex that facilitates the flexion of the joint and enables the animal to walk. Right: A drawing of a stick insect showing the location of the femur and the tibia.

One way in which the femoral chordotonal organ contributes to the control of leg movement is through a resistance reflex, in which a sub-group of femoral chordotonal neurons sense the extension of the tibia and activates the motor neurons that flexes tibia to counteract the movement (Figure 3).[4] During walking, this stabilization reflex is reversed in order to promote the cyclic flexion and extension of the femur-tibia joint necessary for walking (Figure 3).[20][21]

Biomechanical specialization and feature selectivity

One possible mechanism for determining the feature selectivity of femoral chordotonal neurons is biomechanical specialization that transmit distinct forces to each type of proprioceptors, or distribute forces differently to proprioceptors in different locations. For position sensing claw cells of Drosophila, it has been shown that biomechanical properties of the tendon, surrounding tissues, and dendrites lead to different amount of strain generated on the dendrite of a claw cell depending on where the cell is located along the femur.[22] This gradient of strain allows claw cells to respond at different tibia angles and generate a topographic map of joint angles in the femoral chordotonal organ.[22]

References

  1. ↑ 1.0 1.1 Field, Laurence H.; Matheson, Thomas (1998-01-01), Evans, P. D., ed. (in en), Chordotonal Organs of Insects, Advances in Insect Physiology, 27, Academic Press, pp. 1–228, doi:10.1016/s0065-2806(08)60013-2, ISBN 9780120242276, https://www.sciencedirect.com/science/article/pii/S0065280608600132, retrieved 2022-02-03 
  2. ↑ 2.0 2.1 BÄSSLER, ULRICH (1988-05-01). "Functional Principles of Pattern Generation for Walking Movements of Stick Insect Forelegs: The Role of the Femoral Chordotonal Organ Afferences". Journal of Experimental Biology 136 (1): 125–147. doi:10.1242/jeb.136.1.125. ISSN 0022-0949. 
  3. ↑ 3.0 3.1 Page, Keri L.; Matheson, Thomas (2009-03-25). "Functional Recovery of Aimed Scratching Movements after a Graded Proprioceptive Manipulation" (in en). Journal of Neuroscience 29 (12): 3897–3907. doi:10.1523/JNEUROSCI.0089-09.2009. ISSN 0270-6474. PMID 19321786. PMC 6665037. https://www.jneurosci.org/content/29/12/3897. 
  4. ↑ 4.0 4.1 FIELD, L.H.; BURROWS, M. (1982-12-01). "Reflex Effects of the Femoral Chordotonal Organ Upon Leg Motor Neurones of the Locust". Journal of Experimental Biology 101 (1): 265–285. doi:10.1242/jeb.101.1.265. ISSN 0022-0949. 
  5. ↑ Mendes, César S; Bartos, Imre; Akay, Turgay; Márka, Szabolcs; Mann, Richard S (2013-01-08). Calabrese, Ron. ed. "Quantification of gait parameters in freely walking wild type and sensory deprived Drosophila melanogaster". eLife 2: e00231. doi:10.7554/eLife.00231. ISSN 2050-084X. PMID 23326642. 
  6. ↑ Shanbhag, Shubha R.; Singh, Kusum; Naresh Singh, R. (1992-10-01). "Ultrastructure of the femoral chordotonal organs and their novel synaptic organization in the legs of Drosophila melanogaster Meigen (Diptera : Drosophilidae)" (in en). International Journal of Insect Morphology and Embryology 21 (4): 311–322. doi:10.1016/0020-7322(92)90026-J. ISSN 0020-7322. https://dx.doi.org/10.1016/0020-7322%2892%2990026-J. 
  7. ↑ Field, Laurence H. (February 1991). "Mechanism for range fractionation in chordotonal organs of Locusta migratoria (L) and Valanga sp. (Orthoptera : Acrididae)" (in en). International Journal of Insect Morphology and Embryology 20 (1–2): 25–39. doi:10.1016/0020-7322(91)90025-5. https://linkinghub.elsevier.com/retrieve/pii/0020732291900255. 
  8. ↑ SHELTON, P. M.J.; STEPHEN, R. O.; SCOTT, J. J.A.; TINDALL, A. R. (1992-02-01). "The Apodeme Complex of the Femoral Chordotonal Organ in the Metathoracic Leg of the Locust Schistocerca Gregaria". Journal of Experimental Biology 163 (1): 345–358. doi:10.1242/jeb.163.1.345. ISSN 0022-0949. https://doi.org/10.1242/jeb.163.1.345. 
  9. ↑ Nowel, M; Shelton, P; Stephen, R (1995-09-01). "Functional organisation of the metathoracic femoral chordotonal organ in the cricket Acheta domesticus" (in en). Journal of Experimental Biology 198 (9): 1977–1988. doi:10.1242/jeb.198.9.1977. ISSN 1477-9145. PMID 9319888. https://journals.biologists.com/jeb/article/198/9/1977/7112/Functional-organisation-of-the-metathoracic. 
  10. ↑ Theophilidis, G (1986-01-01). "The femoral chordotonal organs of Decticus albifrons (Orthoptera: Tettigoniidae)—I. Structure" (in en). Comparative Biochemistry and Physiology Part A: Physiology 84 (3): 529–536. doi:10.1016/0300-9629(86)90361-0. ISSN 0300-9629. https://dx.doi.org/10.1016/0300-9629%2886%2990361-0. 
  11. ↑ 11.0 11.1 11.2 11.3 Mamiya, Akira; Gurung, Pralaksha; Tuthill, John C. (2018-11-07). "Neural Coding of Leg Proprioception in Drosophila" (in English). Neuron 100 (3): 636–650.e6. doi:10.1016/j.neuron.2018.09.009. ISSN 0896-6273. PMID 30293823. 
  12. ↑ 12.0 12.1 Phillis, R.; Statton, D.; Caruccio, P.; Murphey, R.K. (1996-10-01). "Mutations in the 8 kDa dynein light chain gene disrupt sensory axon projections in the Drosophila imaginal CNS". Development 122 (10): 2955–2963. doi:10.1242/dev.122.10.2955. ISSN 0950-1991. PMID 8898210. https://doi.org/10.1242/dev.122.10.2955. 
  13. ↑ Field, L. H.; Pflüger, H. -J. (1989-01-01). "The femoral chordotonal organ: A bifunctional orthopteran (Locusta migratoria) sense organ?" (in en). Comparative Biochemistry and Physiology Part A: Physiology 93 (4): 729–743. doi:10.1016/0300-9629(89)90494-5. ISSN 0300-9629. https://dx.doi.org/10.1016/0300-9629%2889%2990494-5. 
  14. ↑ Hofmann, T.; Koch, U. T.; Bässler, U. (1985-01-01). "Physiology of the Femoral Chordotonal Organ in the Stick Insect, Cuniculina Impigra". Journal of Experimental Biology 114 (1): 207–223. doi:10.1242/jeb.114.1.207. ISSN 0022-0949. 
  15. ↑ Kondoh, Y.; Okuma, J.; Newland, P. L. (1995-05-01). "Dynamics of neurons controlling movements of a locust hind leg: Wiener kernel analysis of the responses of proprioceptive afferents". Journal of Neurophysiology 73 (5): 1829–1842. doi:10.1152/jn.1995.73.5.1829. ISSN 0022-3077. PMID 7623084. https://journals.physiology.org/doi/abs/10.1152/jn.1995.73.5.1829. 
  16. ↑ Matheson, Thomas (1990-04-01). "Responses and locations of neurones in the locust metathoracic femoral chordotonal organ" (in en). Journal of Comparative Physiology A 166 (6): 915–927. doi:10.1007/BF00187338. ISSN 1432-1351. https://doi.org/10.1007/BF00187338. 
  17. ↑ Matheson, Thomas (1992-04-01). "Range fractionation in the locust metathoracic femoral chordotonal organ" (in en). Journal of Comparative Physiology A 170 (4): 509–520. doi:10.1007/BF00191466. ISSN 1432-1351. https://doi.org/10.1007/BF00191466. 
  18. ↑ Stein, W.; Sauer, A. E. (1999-04-01). "Physiology of vibration-sensitive afferents in the femoral chordotonal organ of the stick insect" (in en). Journal of Comparative Physiology A 184 (3): 253–263. doi:10.1007/s003590050323. ISSN 1432-1351. https://doi.org/10.1007/s003590050323. 
  19. ↑ Zill, S. N. (1985-05-01). "Plasticity and proprioception in insects. I. Responses and cellular properties of individual receptors of the locust metathoracic femoral chordotonal organ". Journal of Experimental Biology 116 (1): 435–461. doi:10.1242/jeb.116.1.435. ISSN 0022-0949. PMID 4056657. https://doi.org/10.1242/jeb.116.1.435. 
  20. ↑ Bässler, U. (1976-03-01). "Reversal of a reflex to a single motoneuron in the stick insect Çarausius morosus". Biological Cybernetics 24 (1): 47–49. doi:10.1007/bf00365594. ISSN 0340-1200. http://dx.doi.org/10.1007/bf00365594. 
  21. ↑ Zill, S. N. (1985-05-01). "Plasticity and proprioception in insects. II. Modes of reflex action of the locust metathoracic femoral chordotonal organ". Journal of Experimental Biology 116 (1): 463–480. doi:10.1242/jeb.116.1.463. ISSN 1477-9145. PMID 4056658. 
  22. ↑ 22.0 22.1 Mamiya, Akira; Sustar, Anne; Siwanowicz, Igor; Qi, Yanyan; Lu, Tzu-Chiao; Gurung, Pralaksha; Chen, Chenghao; Phelps, Jasper S. et al. (October 2023). "Biomechanical origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg" (in en). Neuron 111 (20): 3230–3243.e14. doi:10.1016/j.neuron.2023.07.009. https://linkinghub.elsevier.com/retrieve/pii/S0896627323005421. 



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