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Homologies of spinal ascending nociceptive pathways between rats and macaques: can we transpose to human? A review and analysis of the literature

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Abstract

Purpose

Due to the difficulty of using neural tracers in humans, knowledge of the nociceptive system’s anatomy is mainly derived from studies in animals and mainly in rats. The aim of this study was to investigate the morphological differences of the ascending spinal nociceptive pathways between the rat and the macaque monkey; in order to evaluate the variability of this anatomy during phylogenesis, and thus to know if the anatomical description of these pathways can be transposed from the rat to the human.

Methods

A review and analysis of the literature were performed. The criteria used for comparison were: origins, pathways, their terminations in target structures, and projections from target structures of ascending spinal nociceptive pathways. The monkey was used as an intermediate species for comparison because of the lack of data in humans. The hypothesis of transposition of anatomy between rat and human was considered rejected if differences were found between rat and monkey.

Results

An anatomical difference in termination was found for the spino-annular or spino-periaqueductal grey (spino-PAG) pathway and transposition of its anatomy from rat to human was rejected. No difference was found in other pathways and the transposition of their anatomy from rat to human was therefore, not rejected.

Conclusion

This work highlights the conservation of most of the ascending spinal nociceptive pathways’ anatomy between rat and monkey. Thus, the possibility for a transposition of their anatomy between rat and human is not rejected.

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Fig. 1

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 2

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 3

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 4

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 5

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 6

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 7

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 8

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 9

Adapted from Paxinos, G. and Watson, C. 1997 The Rat Brain in Stereotaxic Coordinates, 3th edn. Academic Press—with permission. Credit for graphic optimization to V.N Pommier

Fig. 10

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Data availability

All the data are available on PubMed.

References

  1. Molony V, Kent JE (1997) Assessment of acute pain in farm animals using behavioral and physiological measurements. J Anim Sci 75(1):266–272. https://doi.org/10.2527/1997.751266x

    Article  CAS  PubMed  Google Scholar 

  2. Whishaw IQ (2004) The behavior of the laboratory rat: a handbook with tests. Oxford University Press, Oxford

    Book  Google Scholar 

  3. Baker ML, Giesler GJ (1984) Anatomical studies of the spinocervical tract of the rat. Somatosens Res 2:1–18

    Article  CAS  PubMed  Google Scholar 

  4. Giesler GJ, Björkeland M, Xu Q, Grant G (1988) Organization of the spinocervicothalamic pathway in the rat. J Comp Neurol 268:223–233. https://doi.org/10.1002/cne.902680207

    Article  PubMed  Google Scholar 

  5. Ha H, Liu CN (1966) Organization of the spino-cervico-thalamic system. J Comp Neurol 127:445–470. https://doi.org/10.1002/cne.901270403

    Article  CAS  PubMed  Google Scholar 

  6. Willis WD, Coggeshall RE (2004) Sensory mechanisms of the spinal cord: Volume 2 ascending sensory tracts and their descending control. Springer, New York

    Book  Google Scholar 

  7. Almeida TF, Roizenblatt S, Tufik S (2004) Afferent pain pathways: a neuroanatomical review. Brain Res 1000:40–56. https://doi.org/10.1016/j.brainres.2003.10.073

    Article  CAS  PubMed  Google Scholar 

  8. Tavares I, Lima D, Coimbra A (1993) Neurons in the superficial dorsal horn of the rat spinal cord projecting to the medullary ventrolateral reticular formation express c-fos after noxious stimulation of the skin. Brain Res 623:278–286. https://doi.org/10.1016/0006-8993(93)91438-x

    Article  CAS  PubMed  Google Scholar 

  9. Lima D, Coimbra A (1991) Neurons in the substantia gelatinosa rolandi (lamina II) project to the caudal ventrolateral reticular formation of the medulla oblongata in the rat. Neurosci Lett 132:16–18. https://doi.org/10.1016/0304-3940(91)90421-o

    Article  CAS  PubMed  Google Scholar 

  10. Tavares I, Lima D, Coimbra A (1996) The ventrolateral medulla of the rat is connected with the spinal cord dorsal horn by an indirect descending pathway relayed in the A5 noradrenergic cell group. J Comp Neurol 374:84–95. https://doi.org/10.1002/(SICI)1096-9861(19961007)374:1%3c84::AID-CNE6%3e3.0.CO;2-J

    Article  CAS  PubMed  Google Scholar 

  11. Kevetter GA, Haber LH, Yezierski RP, Chung JM, Martin RF, Willis WD (1982) Cells of origin of the spinoreticular tract in the monkey. J Comp Neurol 207:61–74. https://doi.org/10.1002/cne.902070106

    Article  CAS  PubMed  Google Scholar 

  12. Lima D, Coimbra A (1990) Structural types of marginal (lamina I) neurons projecting to the dorsal reticular nucleus of the medulla oblongata. Neuroscience 34:591–606. https://doi.org/10.1016/0306-4522(90)90167-3

    Article  CAS  PubMed  Google Scholar 

  13. Bing Z, Villanueva L, Le Bars D (1990) Ascending pathways in the spinal cord involved in the activation of subnucleus reticularis dorsalis neurons in the medulla of the rat. J Neurophysiol 63:424–438. https://doi.org/10.1152/jn.1990.63.3.424

    Article  CAS  PubMed  Google Scholar 

  14. Almeida A, Tavares I, Lima D (1995) Projection sites of superficial or deep dorsal horn in the dorsal reticular nucleus. NeuroReport 6:1245–1248. https://doi.org/10.1097/00001756-199506090-00004

    Article  CAS  PubMed  Google Scholar 

  15. Almeida A, Tavares I, Lima D (2000) Reciprocal connections between the medullary dorsal reticular nucleus and the spinal dorsal horn in the rat. Eur J Pain 4:373–387. https://doi.org/10.1053/eujp.2000.0193

    Article  CAS  PubMed  Google Scholar 

  16. Bernard JF, Besson JM (1990) The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 63:473–490. https://doi.org/10.1152/jn.1990.63.3.473

    Article  CAS  PubMed  Google Scholar 

  17. Villanueva L, Desbois C, le Bars D, Bernard JF (1998) Organization of diencephalic projections from the medullary subnucleus reticularis dorsalis and the adjacent cuneate nucleus: a retrograde and anterograde tracer study in the rat. J Comp Neurol 390:133–160

    Article  CAS  PubMed  Google Scholar 

  18. Leak J, Menetrey D, De Pommery J (1988) Neuropeptides in long ascending spinal tract cells in the rat: evidence for parallel processing of ascending information. Neuroscience 24:195–207. https://doi.org/10.1016/0306-4522(88)90323-5

    Article  Google Scholar 

  19. Nahin RL, Micevych PE (1986) A long ascending pathway of enkephalin-like immunoreactive spinoreticular neurons in the rat. Neurosci Lett 65:271–276. https://doi.org/10.1016/0304-3940(86)90273-9

    Article  CAS  PubMed  Google Scholar 

  20. Peschanski M, Besson JM (1984) A spino-reticulo-thalamic pathway in the rat: an anatomical study with reference to pain transmission. Neuroscience 12:165–178. https://doi.org/10.1016/0306-4522(84)90145-3

    Article  CAS  PubMed  Google Scholar 

  21. Fields HL, Malick A, Burstein R (1995) Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol 74:1742–1759. https://doi.org/10.1152/jn.1995.74.4.1742

    Article  CAS  PubMed  Google Scholar 

  22. Craig AD (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol 361:225–248. https://doi.org/10.1002/cne.903610204

    Article  CAS  PubMed  Google Scholar 

  23. Haber LH, Moore BD, Willis WD (1982) Electrophysiological response properties of spinoreticular neurons in the monkey. J Comp Neurol 207:75–84. https://doi.org/10.1002/cne.902070107

    Article  CAS  PubMed  Google Scholar 

  24. Menetrey D, De Pommery J (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur J Neurosci 3:249–259. https://doi.org/10.1111/j.1460-9568.1991.tb00087.x

    Article  PubMed  Google Scholar 

  25. Hylden JLK, Anton F, Nahin RL (1989) Spinal lamina I projection neurons in the rat: collateral innervation of parabrachial area and thalamus. Neuroscience 28:27–37. https://doi.org/10.1016/0306-4522(89)90229-7

    Article  CAS  PubMed  Google Scholar 

  26. Slugg RM, Light AR (1994) Spinal cord and trigeminal projections to the pontine parabrachial region in the rat as demonstrated with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 339:49–61. https://doi.org/10.1002/cne.903390106

    Article  CAS  PubMed  Google Scholar 

  27. Spike RC, Puskar Z, Andrew D, Todd AJ (2003) A quantitative and morphological study of projection neurons in lamina I of the rat lumbar spinal cord. Eur J Neurosci 18:2433–2448. https://doi.org/10.1046/j.1460-9568.2003.02981.x

    Article  CAS  PubMed  Google Scholar 

  28. Yezierski RP, Mendez CM (1991) Spinal distribution and collateral projections of rat spinomesencephalic tract cells. Neuroscience 44:113–130. https://doi.org/10.1016/0306-4522(91)90254-l

    Article  CAS  PubMed  Google Scholar 

  29. Yezierski RP (1988) Spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat, and monkey. J Comp Neurol 267:131–146. https://doi.org/10.1002/cne.902670109

    Article  CAS  PubMed  Google Scholar 

  30. Eberhart JA, Morrell JI, Krieger MS, Pfaff DW (1985) An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it, in the rat. J Comp Neurol 241:285–310. https://doi.org/10.1002/cne.902410305

    Article  CAS  PubMed  Google Scholar 

  31. Lovick TA (1993) Integrated activity of cardiovascular and pain regulatory systems: role in adaptive behavioural responses. Prog Neurobiol 40:631–644. https://doi.org/10.1016/0301-0082(93)90036-r

    Article  CAS  PubMed  Google Scholar 

  32. Malick A, Burstein R (1998) Cells of origin of the trigeminohypothalamic tract in the rat. J Comp Neurol 400:125–144. https://doi.org/10.1002/(sici)1096-9861(19981012)400:1%3c125::aid-cne9%3e3.0.co;2-b

    Article  CAS  PubMed  Google Scholar 

  33. Kostarczyk E, Zhang X, Giesler GJ (1997) Spinohypothalamic tract neurons in the cervical enlargement of rats: locations of antidromically identified ascending axons and their collateral branches in the contralateral brain. J Neurophysiol 77:435–451. https://doi.org/10.1152/jn.1997.77.1.435

    Article  CAS  PubMed  Google Scholar 

  34. Gauriau C, Bernard JF (2004) A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. J Comp Neurol 468:24–56. https://doi.org/10.1002/cne.10873

    Article  PubMed  Google Scholar 

  35. Hardy SP (2001) Hypothalamic projections to cardiovascular centers of the medulla. Brain Res 894:233–240. https://doi.org/10.1016/s0006-8993(01)02053-4

    Article  CAS  PubMed  Google Scholar 

  36. Kerr FW (1975) The ventral spinothalamic tract and other ascending systems of the ventral funiculus of the spinal cord. J Comp Neurol 159:335–355. https://doi.org/10.1002/cne.901590304

    Article  CAS  PubMed  Google Scholar 

  37. Zhang X, Wenk HN, Honda CN, Giesler GJ (2000) Locations of spinothalamic tract axons in cervical and thoracic spinal cord white matter in monkeys. J Neurophysiol 83:2869–2880. https://doi.org/10.1152/jn.2000.83.5.2869

    Article  CAS  PubMed  Google Scholar 

  38. Hodge CJ, Apkarian AV (1990) The spinothalamic tract. Crit Rev Neurobiol 5:363–397

    PubMed  Google Scholar 

  39. Craig AD, Bushnell MC, Zhang ET, Blomqvist A (1994) A thalamic nucleus specific for pain and temperature sensation. Nature 372:770–773. https://doi.org/10.1038/372770a0

    Article  CAS  PubMed  Google Scholar 

  40. Willis WD, Zhang X, Honda CN, Giesler GJ (2001) Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. Pain 92:267–276. https://doi.org/10.1016/s0304-3959(01)00268-8

    Article  PubMed  Google Scholar 

  41. Apkarian AV, Hodge CJ (1989) Primate spinothalamic pathways: II. The cells of origin of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 288:474–492. https://doi.org/10.1002/cne.902880308

    Article  CAS  PubMed  Google Scholar 

  42. Craig AD, Burton H (1981) Spinal and medullary lamina I projection to nucleus submedius in medial thalamus: a possible pain center. J Neurophysiol 45:443–466. https://doi.org/10.1152/jn.1981.45.3.443

    Article  PubMed  Google Scholar 

  43. Springer MS, Burk-Herrick A, Meredith R, Eizirik E, Teeling E, O’Brien SJ, Murphy WJ (2007) The adequacy of morphology for reconstructing the early history of placental mammals. Syst Biol 56:673–684. https://doi.org/10.1080/10635150701491149

    Article  PubMed  Google Scholar 

  44. Sneddon LU (2004) Evolution of nociception in vertebrates: comparative analysis of lower vertebrates. Brain Res Brain Res Rev 46:123–130. https://doi.org/10.1016/j.brainresrev.2004.07.007

    Article  CAS  PubMed  Google Scholar 

  45. Bowsher D, Alexinsky T (1980) Introduction à l’anatomie et à la physiologie du système nerveux. Médecine et sciences internationales, Paris

    Google Scholar 

  46. Krinke GJ (2000) The laboratory rat. Elsevier, Amsterdam

    Google Scholar 

  47. Mehler WR (1966) Some observations on secondary ascending afferent systems in the central nervous system. In: Knighton RS, Dumke PR (eds) Pain. Little Brown, Boston, pp 11–32

    Google Scholar 

  48. Burstein R, Giesler GJ (1989) Retrograde labeling of neurons in spinal cord that project directly to nucleus accumbens or the septal nuclei in the rat. Brain Res 497:149–154. https://doi.org/10.1016/0006-8993(89)90981-5

    Article  CAS  PubMed  Google Scholar 

  49. Gamboa-Esteves FO, Tavares I, Almeida A, Batten TF, McWilliam PN, Lima D (2001) Projection sites of superficial and deep spinal dorsal horn cells in the nucleus tractus solitarii of the rat. Brain Res 921:195–205. https://doi.org/10.1016/s0006-8993(01)03118-3

    Article  CAS  PubMed  Google Scholar 

  50. Hong JH, Son SM, Jang SH (2010) Identification of spinothalamic tract and its related thalamocortical fibers in human brain. Neurosci Lett 468:102–105. https://doi.org/10.1016/j.neulet.2009.10.075

    Article  CAS  PubMed  Google Scholar 

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ED: protocol/project development, data collection or management, data analysis, manuscript writing/editing. AG: data analysis, manuscript writing/editing. GF: data analysis, data collection or management. LB: data analysis, data collection or management. BM: data analysis, manuscript writing/editing. OP: protocol/project development, data analysis.

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Correspondence to Eric Dabala.

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Dabala, E., Guédon, A., Ficheux, G. et al. Homologies of spinal ascending nociceptive pathways between rats and macaques: can we transpose to human? A review and analysis of the literature. Surg Radiol Anat 45, 1443–1460 (2023). https://doi.org/10.1007/s00276-023-03212-w

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