Biology:Campaniform sensilla

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Short description: Class of mechanoreceptors found in insects
Cross-section of a campaniform sensillum. Each sensillum is embedded in a cuticular socket and innervated by a single sensory neuron. The neuron is excited when strain in the cuticle deforms the socket edges (collar) and indents the flexible cuticular dome (cap).

File:Campaniforms on leg and haltere.tif Campaniform sensilla are a class of mechanoreceptors found in insects, which respond to local stress and strain within the animal's cuticle. Campaniform sensilla function as proprioceptors that detect mechanical load as resistance to muscle contraction,[1][2] similar to mammalian Golgi tendon organs.[3][4] Sensory feedback from campaniform sensilla is integrated in the control of posture and locomotion.[5][6]

Structure

Each campaniform sensillum consists of a flexible dome, which is embedded in a spongy socket within the cuticle and innervated by the dendrites of a single bipolar sensory neuron (see schematic cross-section). Campaniform sensilla are often oval-shaped with long axes of about 5-10 µm (see SEM).

Campaniform sensilla are distributed across the body surface of many insects. The fruit fly Drosophila melanogaster, for example, has over 680 sensilla.[7] Campaniform sensilla are located in regions where stress is likely to be high, including on the legs, antennae, wings, and halteres.[7][8][9] Sensilla may occur alone, but sensilla with similar orientations are often grouped together.

Distribution of groups of campaniform sensilla on a stick insect leg (anterior view). The inset shows a top view of the two groups on the dorsal trochanter (G3 and G4). The sensilla of these groups have mutually perpendicular orientations. Each sensillum is preferentially excited by compression along its short axis (arrows). The proximal group (G3) is oriented perpendicularly to the long axis of the trochanter and excited when the trochanter-femur is bent upwards. The more distal group (G4) is oriented in parallel to the long axis of the trochanter and excited when the trochanter-femur is bent downwards.

Campaniform sensilla on legs

On the legs, groups of campaniform sensilla are located close to the joints on all segments except for the coxa (see leg schematic), with most sensilla located on the proximal trochanter.[10] The number and location of sensilla on the legs varies little across individuals of the same species,[7] and homologous groups of sensilla can be found across species.[10]

Campaniform sensilla on wings and halteres

Distribution of campaniform sensilla (CS) on the wing and haltere of Drosophila melanogaster. Adapted from Aiello et al. (2021).[9]

Campaniform sensilla typically occur on both sides of the wing (see wing schematic). The exact number and placement varies widely across species, likely mirroring differences in flight behavior.[9] However, across species, most campaniform sensilla are found near the wing base.[9] Computational models predict that this is an optimal location for sensing body rotations during flight, with sensing performance being robust to external perturbations and sensor loss.[11]

In Diptera such as Drosophila, the highest density of campaniform sensilla is found at the base of the modified hind-wings, the halteres (see haltere schematic).[7][8]

Function

Response properties

When cuticular deformations compress a campaniform sensillum, the socket edges (collar) indent the cuticular cap.[12] This squeezes the dendritic tip of the sensory neuron and opens its mechanotransduction channels (from the TRP family[13]), which leads to the generation of action potentials that are transmitted to the ventral nerve cord, the insect analogue to the vertebrate spinal cord.

The activity of campaniform sensilla was first recorded by John William Sutton Pringle in the late 1930s.[14] Pringle also determined that the oval shape of many sensilla makes them directionally selective[15] – they respond best to compression along their short axis. Thus, even neighboring sensilla may have very different sensitivities to strain depending on their orientation in the cuticle. For example, stick insects possess two groups of campaniform sensilla on the dorsal side of their legs' trochanter whose short axes are oriented perpendicularly to one another[1] (see inset in leg schematic). As a result, one group (G3) responds when the leg is bent upwards, whereas the other group (G4) responds when the leg is bent downwards. Round campaniform sensilla can be sensitive in all directions[16] or show directional sensitivity if the cap is asymmetrically coupled with the surrounding collar.[17]

The activity of campaniform sensilla may be slowly-adapting (tonic), signaling the magnitude of cuticular deformation, and/or rapidly adapting (phasic), signaling the rate of cuticular deformation.[1][18] Based on their responses to white noise stimuli, campaniform sensilla may also be described more generally as signaling two features that approximate the derivative of each other.[19] This suggests that the neural response properties of the sensilla are rather generic, and that functional specialization arises primarily from how the sensilla are embedded in the cuticle.[19][20] In addition, activity adapts to constant loads and shows hysteresis (history dependence) in response to cyclic loading.[18]

Campaniform sensilla project directly to motor neurons[21] and to various interneurons, which integrate their signals with signals from other proprioceptors.[22] In this way, campaniform sensilla activity can affect the magnitude and timing of muscle contractions.[5]

Function of leg campaniform sensilla

Campaniform sensilla on the legs are activated during standing and walking.[23][24] Their sensory feedback is thought to reinforce muscle activity during the stance phase[1][24][25] and to contribute to inter-leg coordination,[26][27] much like sensory feedback from mammalian Golgi tendon organs.[28][29] Feedback from leg campaniform sensilla is also important for the control of kicking and jumping.[30][31]

Function of wing and haltere campaniform sensilla

Campaniform sensilla on the wings and halteres are activated as these structures oscillate back and forth during flight, with the phase of activation depending on the placement of the sensilla.[9][32] The campaniform sensilla on the wing encode the wing's aerodynamic and inertial forces, whereas sensilla on the base of the haltere are thought to encode Coriolis forces induced by body rotation during flight, allowing the structure to function as a gyroscope.[33] Feedback from wing and haltere campaniform sensilla is thought to mediate compensatory reflexes to maintain equilibrium during flight.[34][35]

Computational models

To better understand the function of campaniform sensilla, computational models that mimic their response properties are being developed for use in simulations and robotics.[36][37] On robotic legs, the models can filter input from engineered strain sensors "campaniform-sensilla-style" in real time.[38] One advantage of this bio-inspired filtering is that it enables adaptation to load over time (see above), which makes strain sensors essentially self-calibrating to different loads carried by the robot.[38]

References

  1. ↑ 1.0 1.1 1.2 1.3 "Force encoding in stick insect legs delineates a reference frame for motor control". Journal of Neurophysiology 108 (5): 1453–72. September 2012. doi:10.1152/jn.00274.2012. PMID 22673329. 
  2. ↑ "Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla, including receptors with round cuticular caps". Arthropod Structure & Development 42 (6): 455–467. November 2013. doi:10.1016/j.asd.2013.10.001. PMID 24126203. 
  3. ↑ "Load-regulating mechanisms in gait and posture: comparative aspects". Physiological Reviews 80 (1): 83–133. January 2000. doi:10.1152/physrev.2000.80.1.83. PMID 10617766. 
  4. ↑ "Proprioception" (in en). Current Biology 28 (5): R194–R203. March 2018. doi:10.1016/j.cub.2018.01.064. PMID 29510103. 
  5. ↑ 5.0 5.1 "Load sensing and control of posture and locomotion". Arthropod Structure & Development 33 (3): 273–86. July 2004. doi:10.1016/j.asd.2004.05.005. PMID 18089039. 
  6. ↑ "Mechanosensation and Adaptive Motor Control in Insects". Current Biology 26 (20): R1022–R1038. October 2016. doi:10.1016/j.cub.2016.06.070. PMID 27780045. 
  7. ↑ 7.0 7.1 7.2 7.3 "Location and arrangement of campaniform sensilla in Drosophila melanogaster". The Journal of Comparative Neurology 529 (4): 905–925. July 2020. doi:10.1002/cne.24987. PMID 32678470. 
  8. ↑ 8.0 8.1 Agrawal, Sweta; Grimaldi, David; Fox, Jessica L. (2017-03-01). "Haltere morphology and campaniform sensilla arrangement across Diptera" (in en). Arthropod Structure & Development 46 (2): 215–229. doi:10.1016/j.asd.2017.01.005. ISSN 1467-8039. PMID 28161605. 
  9. ↑ 9.0 9.1 9.2 9.3 9.4 Aiello, Brett R.; Stanchak, Kathryn E.; Weber, Alison I.; Deora, Tanvi; Sponberg, Simon; Brunton, Bingni W. (2021-06-24). "Spatial distribution of campaniform sensilla mechanosensors on wings: Form, function, and phylogeny" (in en). Current Opinion in Insect Science 48: 8–17. doi:10.1016/j.cois.2021.06.002. ISSN 2214-5745. PMID 34175464. 
  10. ↑ 10.0 10.1 "Gradients in mechanotransduction of force and body weight in insects". Arthropod Structure & Development 58: 100970. September 2020. doi:10.1016/j.asd.2020.100970. PMID 32702647. 
  11. ↑ Weber, Alison I.; Daniel, Thomas L.; Brunton, Bingni W. (2021-08-11). Webb, Barbara. ed. "Wing structure and neural encoding jointly determine sensing strategies in insect flight" (in en). PLOS Computational Biology 17 (8): e1009195. doi:10.1371/journal.pcbi.1009195. ISSN 1553-7358. PMID 34379622. Bibcode: 2021PLSCB..17E9195W. 
  12. ↑ "Proprioceptive indentation of the campaniform sensilla of cockroach legs" (in en). Journal of Comparative Physiology 96 (3): 257–272. 1975-09-01. doi:10.1007/BF00612698. ISSN 1432-1351. 
  13. ↑ "NOMPC, a member of the TRP channel family, localizes to the tubular body and distal cilium of Drosophila campaniform and chordotonal receptor cells". Cytoskeleton 68 (1): 1–7. January 2011. doi:10.1002/cm.20493. PMID 21069788. 
  14. ↑ "Proprioception in insects I. A new type of mechanical receptor from the palps of the cockroach". Journal of Experimental Biology 15 (1): 101–113. 1938. doi:10.1242/jeb.15.1.101. http://jeb.biologists.org/content/15/1/101. 
  15. ↑ "Proprioception in insects II. The action of the campaniform sensilla on the legs". Journal of Experimental Biology 15 (1): 114–131. 1938. doi:10.1242/jeb.15.1.114. http://jeb.biologists.org/content/15/1/114. 
  16. ↑ "Directional Sensitivity and Mechanical Coupling Dynamics of Campaniform Sensilla During Chordwise Deformations of the Fly Wing" (in en). Journal of Experimental Biology 169 (1): 221–233. 1992-08-01. doi:10.1242/jeb.169.1.221. ISSN 0022-0949. https://jeb.biologists.org/content/169/1/221. 
  17. ↑ "Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus". Journal of Comparative Physiology A: Neuroethology, Sensory, Neural & Behavioral Physiology 197 (8): 851–67. August 2011. doi:10.1007/s00359-011-0647-4. PMID 21544617. 
  18. ↑ 18.0 18.1 "Encoding of forces by cockroach tibial campaniform sensilla: implications in dynamic control of posture and locomotion". Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 186 (4): 359–74. April 2000. doi:10.1007/s003590050436. PMID 10798724. https://doi.org/10.1007/s003590050436. 
  19. ↑ 19.0 19.1 Dickerson, Bradley H.; Fox, Jessica L.; Sponberg, Simon (2020-11-28). "Functional diversity from generic encoding in insect campaniform sensilla" (in en). Current Opinion in Physiology 19: 194–203. doi:10.1016/j.cophys.2020.11.004. ISSN 2468-8673. 
  20. ↑ Dinges, Gesa F.; Bockemühl, Till; Iacoviello, Francesco; Shearing, Paul R.; Büschges, Ansgar; Blanke, Alexander (May 2022). "Ultra high-resolution biomechanics suggest that substructures within insect mechanosensors decisively affect their sensitivity" (in en). Journal of the Royal Society Interface 19 (190): 20220102. doi:10.1098/rsif.2022.0102. ISSN 1742-5662. PMID 35506211. 
  21. ↑ Phelps, Jasper S.; Hildebrand, David Grant Colburn; Graham, Brett J.; Kuan, Aaron T.; Thomas, Logan A.; Nguyen, Tri M.; Buhmann, Julia; Azevedo, Anthony W. et al. (2021-02-04). "Reconstruction of motor control circuits in adult Drosophila using automated transmission electron microscopy" (in en). Cell 184 (3): 759–774.e18. doi:10.1016/j.cell.2020.12.013. ISSN 0092-8674. PMID 33400916. 
  22. ↑ Gebehart, Corinna; Schmidt, Joachim; Büschges, Ansgar (2021-05-01). "Distributed processing of load and movement feedback in the premotor network controlling an insect leg joint". Journal of Neurophysiology 125 (5): 1800–1813. doi:10.1152/jn.00090.2021. ISSN 0022-3077. PMID 33788591. https://journals.physiology.org/doi/full/10.1152/jn.00090.2021. 
  23. ↑ Keller, Bridget R.; Duke, Elizabeth R.; Amer, Ayman S.; Zill, Sasha N. (August 2007). "Tuning posture to body load: decreases in load produce discrete sensory signals in the legs of freely standing cockroaches". Journal of Comparative Physiology A: Neuroethology, Sensory, Neural & Behavioral Physiology 193 (8): 881–891. doi:10.1007/s00359-007-0241-y. ISSN 0340-7594. PMID 17541783. https://pubmed.ncbi.nlm.nih.gov/17541783/. 
  24. ↑ 24.0 24.1 "Central Programming and Reflex Control of Walking in the Cockroach" (in en). Journal of Experimental Biology 56 (1): 173–193. 1972. doi:10.1242/jeb.56.1.173. ISSN 0022-0949. http://jeb.biologists.org/content/56/1/173. 
  25. ↑ "Force feedback reinforces muscle synergies in insect legs". Arthropod Structure & Development 44 (6 Pt A): 541–53. November 2015. doi:10.1016/j.asd.2015.07.001. PMID 26193626. 
  26. ↑ "Sensory signals of unloading in one leg follow stance onset in another leg: transfer of load and emergent coordination in cockroach walking". Journal of Neurophysiology 101 (5): 2297–304. May 2009. doi:10.1152/jn.00056.2009. PMID 19261716. 
  27. ↑ "A load-based mechanism for inter-leg coordination in insects". Proceedings. Biological Sciences 284 (1868): 20171755. December 2017. doi:10.1098/rspb.2017.1755. PMID 29187626. 
  28. ↑ "Role of sensory feedback in the control of stance duration in walking cats". Brain Research Reviews. Networks in Motion 57 (1): 222–7. January 2008. doi:10.1016/j.brainresrev.2007.06.014. PMID 17761295. 
  29. ↑ "Computer simulation of stepping in the hind legs of the cat: an examination of mechanisms regulating the stance-to-swing transition". Journal of Neurophysiology 94 (6): 4256–68. December 2005. doi:10.1152/jn.00065.2005. PMID 16049149. 
  30. ↑ "Positive feedback loops from proprioceptors involved in leg movements of the locust" (in en). Journal of Comparative Physiology A 163 (4): 425–440. 1988-07-01. doi:10.1007/BF00604897. 
  31. ↑ "Proprioceptive feedback in locust kicking and jumping during maturation". Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 179 (2): 195–205. August 1996. doi:10.1007/BF00222786. PMID 8765558. 
  32. ↑ DICKINSON, MICHAEL H. (1990-07-01). "Comparison of Encoding Properties of Campaniform Sensilla on the Fly Wing". Journal of Experimental Biology 151 (1): 245–261. doi:10.1242/jeb.151.1.245. ISSN 0022-0949. https://doi.org/10.1242/jeb.151.1.245. 
  33. ↑ Pringle, John William Sutton; Gray, James (1948-11-02). "The gyroscopic mechanism of the halteres of Diptera". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 233 (602): 347–384. doi:10.1098/rstb.1948.0007. Bibcode: 1948RSPTB.233..347P. 
  34. ↑ "Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 354 (1385): 903–16. May 1999. doi:10.1098/rstb.1999.0442. PMID 10382224. 
  35. ↑ "Convergent mechanosensory input structures the firing phase of a steering motor neuron in the blowfly, Calliphora". Journal of Neurophysiology 82 (4): 1916–26. October 1999. doi:10.1152/jn.1999.82.4.1916. PMID 10515981. 
  36. ↑ Szczecinski, Nicholas S.; Zill, Sasha N.; Dallmann, Chris J.; Quinn, Roger D. (2020). "Modeling the Dynamic Sensory Discharges of Insect Campaniform Sensilla". in Vouloutsi, Vasiliki; Mura, Anna; Tauber, Falk et al. (in en). Biomimetic and Biohybrid Systems. Lecture Notes in Computer Science. 12413. Cham: Springer International Publishing. pp. 342–353. doi:10.1007/978-3-030-64313-3_33. ISBN 978-3-030-64313-3. https://link.springer.com/chapter/10.1007/978-3-030-64313-3_33. 
  37. ↑ Goldsmith, C. A.; Szczecinski, N. S.; Quinn, R. D. (2020-09-14). "Neurodynamic modeling of the fruit fly Drosophila melanogaster". Bioinspiration & Biomimetics 15 (6): 065003. doi:10.1088/1748-3190/ab9e52. ISSN 1748-3190. PMID 32924978. https://pubmed.ncbi.nlm.nih.gov/32924978/. 
  38. ↑ 38.0 38.1 Zyhowski, William P.; Zill, Sasha N.; Szczecinski, Nicholas S. (2023). "Adaptive load feedback robustly signals force dynamics in robotic model of Carausius morosus stepping". Frontiers in Neurorobotics 17. doi:10.3389/fnbot.2023.1125171. ISSN 1662-5218. PMID 36776993. 

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