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. (July 21, 2008). "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 (October 9, 2010). "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. hdl:20.500.11937/30100. ISSN 1863-2653. LCCN 2007243247. OCLC 804279700. PMID 20936329. S2CID 1880945.
  3. ^ a b Leiras, Roberto; Cregg, Jared M.; Kiehn, Ole (July 8, 2022). "Brainstem Circuits for Locomotion". Annual Review of Neuroscience. 45 (1): annurev–neuro–082321-025137. doi:10.1146/annurev-neuro-082321-025137. ISSN 0147-006X. PMID 34985919. S2CID 245771230.
  4. ^ Namiki, Shigehiro; Dickinson, Michael H; Wong, Allan M; Korff, Wyatt; Card, Gwyneth M (June 26, 2018). Scott, Kristin (ed.). "The functional organization of descending sensory-motor pathways in Drosophila". eLife. 7: e34272. doi:10.7554/eLife.34272. ISSN 2050-084X. PMC 6019073. PMID 29943730.
  5. ^ Okada, Ryuichi; Sakura, Midori; Mizunami, Makoto (March 31, 2003). "Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain". The Journal of Comparative Neurology. 458 (2): 158–174. doi:10.1002/cne.10580. ISSN 0021-9967. PMID 12596256. S2CID 14396370.
  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". Journal of Comparative Physiology A. 192 (9): 1003–1020. doi:10.1007/s00359-006-0135-4. ISSN 0340-7594. PMID 16733727. S2CID 28032937.
  7. ^ Hsu, Cynthia T.; Bhandawat, Vikas (April 2016). "Organization of descending neurons in Drosophila melanogaster". Scientific Reports. 6 (1): 20259. Bibcode:2016NatSR...620259H. doi:10.1038/srep20259. ISSN 2045-2322. PMC 4738306. PMID 26837716.
  8. ^ a b Namiki, Shigehiro; Dickinson, Michael H; Wong, Allan M; Korff, Wyatt; Card, Gwyneth M (June 26, 2018). "The functional organization of descending sensory-motor pathways in Drosophila". eLife. 7: e34272. doi:10.7554/eLife.34272. ISSN 2050-084X. PMC 6019073. PMID 29943730.
  9. ^ Bidaye, Salil S.; Laturney, Meghan; Chang, Amy K.; Liu, Yuejiang; Bockemühl, Till; Büschges, Ansgar; Scott, Kristin (November 11, 2020). "Two Brain Pathways Initiate Distinct Forward Walking Programs in Drosophila". Neuron. 108 (3): 469–485.e8. doi:10.1016/j.neuron.2020.07.032. ISSN 0896-6273. PMC 9435592. PMID 32822613. S2CID 221198570.
  10. ^ a b Capelli, Paolo; Pivetta, Chiara; Soledad Esposito, Maria; Arber, Silvia (November 2017). "Locomotor speed control circuits in the caudal brainstem". Nature. 551 (7680): 373–377. Bibcode:2017Natur.551..373C. doi:10.1038/nature24064. ISSN 1476-4687. PMID 29059682. S2CID 205260887.
  11. ^ Zacarias, Ricardo; Namiki, Shigehiro; Card, Gwyneth M.; Vasconcelos, Maria Luisa; Moita, Marta A. (September 12, 2018). "Speed dependent descending control of freezing behavior in Drosophila melanogaster". Nature Communications. 9 (1): 3697. Bibcode:2018NatCo...9.3697Z. doi:10.1038/s41467-018-05875-1. ISSN 2041-1723. PMC 6135764. PMID 30209268.
  12. ^ Bouvier, Julien; Caggiano, Vittorio; Leiras, Roberto; Caldeira, Vanessa; Bellardita, Carmelo; Balueva, Kira; Fuchs, Andrea; Kiehn, Ole (November 19, 2015). "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. PMC 4899047. PMID 26590422.
  13. ^ Severi, Kristen E.; Portugues, Ruben; Marques, João C.; O’Malley, Donald M.; Orger, Michael B.; Engert, Florian (August 6, 2014). "Neural Control and Modulation of Swimming Speed in the Larval Zebrafish". Neuron. 83 (3): 692–707. doi:10.1016/j.neuron.2014.06.032. ISSN 0896-6273. PMC 4126853. PMID 25066084.
  14. ^ Namiki, Shigehiro; Ros, Ivo G.; Morrow, Carmen; Rowell, William J.; Card, Gwyneth M.; Korff, Wyatt; Dickinson, Michael H. (March 14, 2022). "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. PMC 9206711. PMID 35090590. S2CID 236961767.
  15. ^ Cregg, Jared M.; Leiras, Roberto; Montalant, Alexia; Wanken, Paulina; Wickersham, Ian R.; Kiehn, Ole (June 2020). "Brainstem neurons that command mammalian locomotor asymmetries". Nature Neuroscience. 23 (6): 730–740. doi:10.1038/s41593-020-0633-7. ISSN 1546-1726. PMC 7610510. 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". Nature Neuroscience. 11 (3): 327–333. doi:10.1038/nn2048. ISSN 1546-1726. PMC 2894808. PMID 18264094.
  17. ^ Schnell, Bettina; Ros, Ivo G.; Dickinson, Michael H. (April 24, 2017). "A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila". Current Biology. 27 (8): 1200–1205. doi:10.1016/j.cub.2017.03.004. ISSN 0960-9822. PMC 6309624. PMID 28392112. S2CID 5052663.
  18. ^ Rayshubskiy, Aleksandr; Holtz, Stephen L.; D’Alessandro, Isabel; Li, Anna A.; Vanderbeck, Quinn X.; Haber, Isabel S.; Gibb, Peter W.; Wilson, Rachel I. (July 18, 2020). "Neural circuit mechanisms for steering control in walking Drosophila": 2020.04.04.024703. doi:10.1101/2020.04.04.024703. {{cite journal}}: Cite journal requires |journal= (help)
  19. ^ a b Bidaye, Salil S.; Machacek, Christian; Wu, Yang; Dickson, Barry J. (April 4, 2014). "Neuronal Control of Drosophila Walking Direction". Science. 344 (6179): 97–101. Bibcode:2014Sci...344...97B. doi:10.1126/science.1249964. ISSN 0036-8075. PMID 24700860. S2CID 27815021.
  20. ^ Ruder, Ludwig; Takeoka, Aya; Arber, Silvia (December 7, 2016). "Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability". Neuron. 92 (5): 1063–1078. doi:10.1016/j.neuron.2016.10.032. ISSN 0896-6273. PMID 27866798. S2CID 2203590.
  21. ^ Korn, Henri; Faber, Donald S. (July 7, 2005). "The Mauthner Cell Half a Century Later: A Neurobiological Model for Decision-Making?". Neuron. 47 (1): 13–28. doi:10.1016/j.neuron.2005.05.019. ISSN 0896-6273. PMID 15996545. S2CID 2851487.
  22. ^ Hampel, Stefanie; Franconville, Romain; Simpson, Julie H; Seeds, Andrew M (September 7, 2015). Borst, Alexander (ed.). "A neural command circuit for grooming movement control". eLife. 4: e08758. doi:10.7554/eLife.08758. ISSN 2050-084X. PMC 4599031. PMID 26344548.
  23. ^ Cande, Jessica; Namiki, Shigehiro; Qiu, Jirui; Korff, Wyatt; Card, Gwyneth M; Shaevitz, Joshua W; Stern, David L; Berman, Gordon J (June 26, 2018). "Optogenetic dissection of descending behavioral control in Drosophila". eLife. 7: e34275. doi:10.7554/eLife.34275. ISSN 2050-084X. PMC 6031430. PMID 29943729.
  24. ^ Namiki, Shigehiro; Ros, Ivo G.; Morrow, Carmen; Rowell, William J.; Card, Gwyneth M.; Korff, Wyatt; Dickinson, Michael H. (January 31, 2022). "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 0960-9822. PMC 9206711. PMID 35090590. S2CID 236961767.
  25. ^ Lemon, Roger N. (July 1, 2008). "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.
  26. ^ Jordan, Larry M.; Liu, Jun; Hedlund, Peter B.; Akay, Turgay; Pearson, Keir G. (January 1, 2008). "Descending command systems for the initiation of locomotion in mammals". Brain Research Reviews. Networks in Motion. 57 (1): 183–191. doi:10.1016/j.brainresrev.2007.07.019. ISSN 0165-0173. PMID 17928060. S2CID 39052299.
  27. ^ Bidaye, Salil S.; Bockemühl, Till; Büschges, Ansgar (February 1, 2018). "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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