Biology:Descending neuron

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A descending neuron is a neuron that conveys signals from the brain to neural circuits in the spinal cord (vertebrates) or ventral nerve cord (invertebrates). As the sole conduits of information between the brain and the body, descending neurons play a key role in behavior. Their activity can initiate, maintain, modulate, and terminate behaviors such as locomotion. Because the number of descending neurons is several orders of magnitude smaller than the number of neurons in either the brain or spinal cord/ventral nerve cord, this class of cells represents a critical bottleneck in the flow of information from sensory systems to motor circuits.

Anatomy

Descending neurons have their somas and dendrites (primary input zones) in the brain. Their axons traverse the neck in connectives, or tracts, and output onto neurons in the spinal cord (vertebrates) or ventral nerve cord (invertebrates).

Schematic of major descending pathways in mammals. The corticospinal and corticobulbar tracts are pyramidal tracts controlling voluntary movement. The tectospinal, rubrospinal, vestibulospinal, and reticulospinal tracts are extrapyramidal tracts controlling involuntary movement.

Mammals possess hundreds of thousands of descending neurons.[1][2] They can be divided functionally into two major pathways: pyramidal tracts, which originate in the motor cortex, and extrapyramidal tracts, which originate in the brainstem (see schematic). An example of the former is the corticospinal tract, which is responsible for voluntary movement of the body. An example of the latter is the reticulospinal tract, which contributes to the unconscious regulation of locomotion and posture. Reticulospinal neurons originate in the medullary reticular formation, where they receive information from upstream locomotor centers, such as the mesencephalic locomotor region and the basal ganglia.[3]

Side-view schematic of major descending pathways in Drosophila melanogaster. In the ventral nerve chord, the major pathways target the dorsal wing, neck, and haltere neuropils, the ventral leg neuropils, and the intermediate tectulum, an integrative region. Adapted from Namiki et al. (2018)[4].

Insects possess only several hundreds of descending neurons.[5][6][7][8] Work in the fruit fly Drosophila melanogaster suggests that they are organized into three broad pathways (see schematic).[8] Two direct pathways link specific regions in the brain to motor circuits in the ventral nerve cord controlling the legs and wings, respectively. A third pathway couples a broad array of brain regions to a large integrative region in the ventral nerve cord that may control both sets of appendages.


Function

Descending neurons play an important role in initiating, maintaining, modulating, and terminating behaviors. Several descending neurons involved in controlling specific behaviors have been identified in both vertebrates and invertebrates. These include descending neurons that can initiate and terminate locomotion,[9][10][11][12] modulate locomotion speed[10][13][14] and direction,[15][16][17][18][19] and help coordinate limbs.[20]

While some descending neurons are sufficient to elicit specific behaviors,[21][22][19] most behaviors are likely not controlled by single, command-like descending neurons, but instead by the combined activity of different descending neurons.[23][24]

Some descending pathways form direct connections with motor neurons and premotor interneurons,[25] including central pattern generators.[26] But how exactly descending signals are integrated in circuits in the spinal cord (vertebrates) or ventral nerve cord (invertebrates) during behavior is not well understood.[3][27]

See also

References

  1. ↑ Lemon, Roger N. (2008-07-21). "Descending Pathways in Motor Control". Annual Review of Neuroscience 31: 195–218. doi:10.1146/annurev.neuro.31.060407.125547. ISSN 0147-006X. OCLC 57214750. PMID 18558853. 
  2. ↑ Liang, Huazheng; Paxinos, George; Watson, Charles (2010-10-09). "Projections from the brain to the spinal cord in the mouse". Brain Structure and Function 215 (3–4): 159–186. doi:10.1007/s00429-010-0281-x. ISSN 1863-2653. OCLC 804279700. PMID 20936329. 
  3. ↑ 3.0 3.1 Leiras, Roberto; Cregg, Jared M.; Kiehn, Ole (2022-07-08). "Brainstem Circuits for Locomotion" (in en). Annual Review of Neuroscience 45 (1): annurev–neuro–082321-025137. doi:10.1146/annurev-neuro-082321-025137. ISSN 0147-006X. PMID 34985919. https://www.annualreviews.org/doi/10.1146/annurev-neuro-082321-025137. 
  4. ↑ Namiki, Shigehiro; Dickinson, Michael H; Wong, Allan M; Korff, Wyatt; Card, Gwyneth M (2018-06-26). Scott, Kristin. ed. "The functional organization of descending sensory-motor pathways in Drosophila". eLife 7: e34272. doi:10.7554/eLife.34272. ISSN 2050-084X. PMID 29943730. 
  5. ↑ Okada, Ryuichi; Sakura, Midori; Mizunami, Makoto (2003-03-31). "Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain" (in en). The Journal of Comparative Neurology 458 (2): 158–174. doi:10.1002/cne.10580. ISSN 0021-9967. PMID 12596256. https://onlinelibrary.wiley.com/doi/10.1002/cne.10580. 
  6. ↑ Gal, Ram; Libersat, Frederic (September 2006). "New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia" (in en). Journal of Comparative Physiology A 192 (9): 1003–1020. doi:10.1007/s00359-006-0135-4. ISSN 0340-7594. PMID 16733727. http://link.springer.com/10.1007/s00359-006-0135-4. 
  7. ↑ Hsu, Cynthia T.; Bhandawat, Vikas (April 2016). "Organization of descending neurons in Drosophila melanogaster" (in en). Scientific Reports 6 (1): 20259. doi:10.1038/srep20259. ISSN 2045-2322. PMID 26837716. Bibcode: 2016NatSR...620259H. 
  8. ↑ 8.0 8.1 Namiki, Shigehiro; Dickinson, Michael H; Wong, Allan M; Korff, Wyatt; Card, Gwyneth M (2018-06-26). "The functional organization of descending sensory-motor pathways in Drosophila" (in en). eLife 7: e34272. doi:10.7554/eLife.34272. ISSN 2050-084X. PMID 29943730. 
  9. ↑ Bidaye, Salil S.; Laturney, Meghan; Chang, Amy K.; Liu, Yuejiang; Bockemühl, Till; Büschges, Ansgar; Scott, Kristin (2020-11-11). "Two Brain Pathways Initiate Distinct Forward Walking Programs in Drosophila" (in en). Neuron 108 (3): 469–485.e8. doi:10.1016/j.neuron.2020.07.032. ISSN 0896-6273. PMID 32822613. 
  10. ↑ 10.0 10.1 Capelli, Paolo; Pivetta, Chiara; Soledad Esposito, Maria; Arber, Silvia (November 2017). "Locomotor speed control circuits in the caudal brainstem" (in en). Nature 551 (7680): 373–377. doi:10.1038/nature24064. ISSN 1476-4687. PMID 29059682. Bibcode: 2017Natur.551..373C. https://www.nature.com/articles/nature24064. 
  11. ↑ Zacarias, Ricardo; Namiki, Shigehiro; Card, Gwyneth M.; Vasconcelos, Maria Luisa; Moita, Marta A. (2018-09-12). "Speed dependent descending control of freezing behavior in Drosophila melanogaster" (in en). Nature Communications 9 (1): 3697. doi:10.1038/s41467-018-05875-1. ISSN 2041-1723. PMID 30209268. Bibcode: 2018NatCo...9.3697Z. 
  12. ↑ Bouvier, Julien; Caggiano, Vittorio; Leiras, Roberto; Caldeira, Vanessa; Bellardita, Carmelo; Balueva, Kira; Fuchs, Andrea; Kiehn, Ole (2015-11-19). "Descending Command Neurons in the Brainstem that Halt Locomotion". Cell 163 (5): 1191–1203. doi:10.1016/j.cell.2015.10.074. ISSN 1097-4172. PMID 26590422. 
  13. ↑ Severi, Kristen E.; Portugues, Ruben; Marques, João C.; O’Malley, Donald M.; Orger, Michael B.; Engert, Florian (2014-08-06). "Neural Control and Modulation of Swimming Speed in the Larval Zebrafish" (in en). Neuron 83 (3): 692–707. doi:10.1016/j.neuron.2014.06.032. ISSN 0896-6273. PMID 25066084. 
  14. ↑ Namiki, Shigehiro; Ros, Ivo G.; Morrow, Carmen; Rowell, William J.; Card, Gwyneth M.; Korff, Wyatt; Dickinson, Michael H. (2022-03-14). "A population of descending neurons that regulates the flight motor of Drosophila". Current Biology 32 (5): 1189–1196.e6. doi:10.1016/j.cub.2022.01.008. ISSN 1879-0445. PMID 35090590. 
  15. ↑ Cregg, Jared M.; Leiras, Roberto; Montalant, Alexia; Wanken, Paulina; Wickersham, Ian R.; Kiehn, Ole (June 2020). "Brainstem neurons that command mammalian locomotor asymmetries" (in en). Nature Neuroscience 23 (6): 730–740. doi:10.1038/s41593-020-0633-7. ISSN 1546-1726. PMID 32393896. 
  16. ↑ Orger, Michael B.; Kampff, Adam R.; Severi, Kristen E.; Bollmann, Johann H.; Engert, Florian (March 2008). "Control of visually guided behavior by distinct populations of spinal projection neurons" (in en). Nature Neuroscience 11 (3): 327–333. doi:10.1038/nn2048. ISSN 1546-1726. PMID 18264094. 
  17. ↑ Schnell, Bettina; Ros, Ivo G.; Dickinson, Michael H. (2017-04-24). "A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila" (in en). Current Biology 27 (8): 1200–1205. doi:10.1016/j.cub.2017.03.004. ISSN 0960-9822. PMID 28392112. 
  18. ↑ Rayshubskiy, Aleksandr; Holtz, Stephen L.; D’Alessandro, Isabel; Li, Anna A.; Vanderbeck, Quinn X.; Haber, Isabel S.; Gibb, Peter W.; Wilson, Rachel I. (2020-07-18) (in en). Neural circuit mechanisms for steering control in walking Drosophila. pp. 2020.04.04.024703. doi:10.1101/2020.04.04.024703. https://www.biorxiv.org/content/10.1101/2020.04.04.024703v2. 
  19. ↑ 19.0 19.1 Bidaye, Salil S.; Machacek, Christian; Wu, Yang; Dickson, Barry J. (2014-04-04). "Neuronal Control of Drosophila Walking Direction" (in en). Science 344 (6179): 97–101. doi:10.1126/science.1249964. ISSN 0036-8075. PMID 24700860. Bibcode: 2014Sci...344...97B. https://www.science.org/doi/10.1126/science.1249964. 
  20. ↑ Ruder, Ludwig; Takeoka, Aya; Arber, Silvia (2016-12-07). "Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability" (in en). Neuron 92 (5): 1063–1078. doi:10.1016/j.neuron.2016.10.032. ISSN 0896-6273. PMID 27866798. 
  21. ↑ Korn, Henri; Faber, Donald S. (2005-07-07). "The Mauthner Cell Half a Century Later: A Neurobiological Model for Decision-Making?" (in en). Neuron 47 (1): 13–28. doi:10.1016/j.neuron.2005.05.019. ISSN 0896-6273. PMID 15996545. 
  22. ↑ Hampel, Stefanie; Franconville, Romain; Simpson, Julie H; Seeds, Andrew M (2015-09-07). Borst, Alexander. ed. "A neural command circuit for grooming movement control". eLife 4: e08758. doi:10.7554/eLife.08758. ISSN 2050-084X. PMID 26344548. 
  23. ↑ Cande, Jessica; Namiki, Shigehiro; Qiu, Jirui; Korff, Wyatt; Card, Gwyneth M; Shaevitz, Joshua W; Stern, David L; Berman, Gordon J (2018-06-26). "Optogenetic dissection of descending behavioral control in Drosophila" (in en). eLife 7: e34275. doi:10.7554/eLife.34275. ISSN 2050-084X. PMID 29943729. 
  24. ↑ Namiki, Shigehiro; Ros, Ivo G.; Morrow, Carmen; Rowell, William J.; Card, Gwyneth M.; Korff, Wyatt; Dickinson, Michael H. (2022-01-31). "A population of descending neurons that regulates the flight motor of Drosophila" (in en). Current Biology 32 (5): 1189–1196.e6. doi:10.1016/j.cub.2022.01.008. ISSN 0960-9822. PMID 35090590. 
  25. ↑ Lemon, Roger N. (2008-07-01). "Descending Pathways in Motor Control". Annual Review of Neuroscience 31 (1): 195–218. doi:10.1146/annurev.neuro.31.060407.125547. ISSN 0147-006X. PMID 18558853. https://www.annualreviews.org/doi/10.1146/annurev.neuro.31.060407.125547. 
  26. ↑ Jordan, Larry M.; Liu, Jun; Hedlund, Peter B.; Akay, Turgay; Pearson, Keir G. (2008-01-01). "Descending command systems for the initiation of locomotion in mammals" (in en). Brain Research Reviews. Networks in Motion 57 (1): 183–191. doi:10.1016/j.brainresrev.2007.07.019. ISSN 0165-0173. PMID 17928060. https://www.sciencedirect.com/science/article/pii/S0165017307001427. 
  27. ↑ Bidaye, Salil S.; Bockemühl, Till; Büschges, Ansgar (2018-02-01). "Six-legged walking in insects: how CPGs, peripheral feedback, and descending signals generate coordinated and adaptive motor rhythms". Journal of Neurophysiology 119 (2): 459–475. doi:10.1152/jn.00658.2017. ISSN 1522-1598. PMID 29070634. 



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