Somatosensory Crossmodal Plasticity in Superior Colliculus of Visually Deafferented Rats
Main Article Content
Abstract
Terminal fields of a certain pathway result denervated if the regeneration after the lesion of the pathway fails. If the lesion happened in a young animal, terminal fields of other nervous pathways that are spatially coincident or are close to the denervated field, growth of axon collaterals or reactive synaptogenesis could take place and reinervate deafferented neurons. In that way these denervated neurons can be recruited for functional compensatory responses and can convey information to areas that result enriched with additional inputs to be processed. The present paper reviews the plastic reactions that take place in the superior colliculus, a mesencephalic layered structure, after the neonatal suppression of its visual afferents that terminate in its superficial layers. The postlesional reactive ascending growth of somatosensory afferents that in control animals innervate intermediate and deep collicular layers invade the superficial layers and connect with visually deafferented cells that result recruited for descendent collicular responses and to send sensory information to the visual cortex via the colliculo-geniculate payhway. In that way in neonatally deafferented animals, somatosensory information gains additional territory to be processed. Two somatosensory connections to the superior collicuus will be discussed in this review. One ascending from the cuneitorm nucleus and the other descending that originates in the barrel cortex.
Article Details
How to Cite
MILLAN, Luis Martinez; CHARAVEN, Juan Carlos.
Somatosensory Crossmodal Plasticity in Superior Colliculus of Visually Deafferented Rats.
Medical Research Archives, [S.l.], v. 9, n. 5, may 2021.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2432>. Date accessed: 21 nov. 2024.
doi: https://doi.org/10.18103/mra.v9i5.2432.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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20. Mooney RD, Nikoletseas MM, King TD, Savage SV, Weaver MT, Rhoades RW. Structural and functional consequences of neonatal deafferentiation in the superficial layers of the hamster’s superior colliculus. J Comp Neurol 1992. 315:398–412.
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26. Staiger JF, Bisler S, Schleicher A, et al Exploration of a novel environment leads to the expression of inducible transcription factors in barrel-related columns. Neuroscience 2000 99:7–16.
27. Staiger JF, Masanneck C, Bisler S et al Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment. Neuroscience 2002 109:687–699.
28. Bisler S, Schleicher A, Gass P et al Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-tobarrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment. J Chem Neuroanat 2002 23:187–198.
29. Mana S, Chevalier G Honeycomb-like structure of the intermediate layers of the rat superior colliculus: afferent and efferent connections. Neuroscience 2001 103:673–693.
30. Lee PH, Helms MC, Augustine GJ, Hall WC Role of intrinsic synaptic circuitry in collicular sensorimotor integration. Proc Natl Acad Sci U S A 1997 94:13299–13304.
31. Isa T, Endo T, Saito Y The visuo-motor pathway in the local circuit of the rat superior colliculus. J Neurosci 1998 18:8496–8504.
32. Ozen G, Augustine GJ, Hall WC Contribution of superficial layer neurons to premotor bursts in the superior colliculus. J Neurophysiol 2000 84:460–471.
33. Helms MC, Ozen G, Hall WC Organization of the intermediate gray layer of the superior colliculus. I. Intrinsic vertical connections. J Neurophysiol 2004 91:1706–1715.
34. Perry VH A tectocortical visual pathway in the rat. Neuroscience 1980 5:915–927.
35. Harting JK, Huerta MF, Hashikawa T, van Lieshout DP Projection of the mammlian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J Comp Neurol 1991 304:275–306.
36. Mundiñano IC and Martinez-Millan L Somatosensory cross-modal plasticity in the superior colliculus of the visually deafferented rats. Neuroscience 2010 165:1457-1470.
37. Toldi J, Rojik I, Feher O Neonatal monocular enucleationinduced cross-modal effects observed in the cortex of adult rat. Neuroscience 1994 62:105–114.
38. Volgyi B, Farkas T, Toldi J Compensation of a sensory deficit inflicted upon newborn and adult animals. A behavioural study. Neuroreport 1993 4:827–829.
2. Dean P, Redgrave P, Westby GWM. Event or emergency? Two response systems in the mammalian superior colliculus. 1989. Trends Neurosci 12:137–147.
3. B.E. Stein, M.A. Meredith, The Merging of the Senses, A Bradford Book, Cambridge, MA, 1993, 211 pp.
4. Benedetti F. Orienting behaviour and superior colliculus sensory representations in mice with the vibrissae bent into the contralateral hemispace. Eur J Neurosci 1995. 7:1512–1519
5. Huerta MF, Harting JK. Connectional organization of the superior colliculus. Trends Neurosci 1984a 7:296-289.
6. Huerta MF, Harting JK. The mammalian superior colliculus: studies of morphology and connections. In: Comparative neurology of the optic tectum (Vanegas H). New York: Plenum Press. 1984b. pp 687–773
7. Garcia Del Cano G, Uria I, Gerrikagoitia I, Martinez-Millan L.Connection from the dorsal column nuclei to the superior colliculus in the rat: topographical organization and somatotopic specific plasticity in response to neonatal enucleation. J Comp Neurol 2004. 468:410–424.
8. Rhoades RW. Effects of neonatal enucleation on the functional organization of the superior colliculus in the golden hamster. J Physiol 1980. 301:383–399.
9. Chow KL, Mathers LH, Spear PD. Spreading of uncrossed retinal projection in superior colliculus of neonatally enucleated rabbits. J Comp Neurol 1973 151:307–322.
10. Lund RD, Lund JS. Reorganization of the retinotectal pathway in rats after neonatal retinal lesions. Exp Neurol 1973 40:377–390.
11. Rhoades RW, DellaCroce DD, Meadows I. Reorganization of somatosensory input to superior colliculus in neonatally enucleated hamsters: anatomical and electrophysiological experiments. J Neurophysiol 1981. 46: 855–877.
12. Rhoades RW, Hess A. Altered catecholaminergic innervation of superior colliculus after enucleation in adult and neonatal hamsters. Brain Res 1983 261:353–357.
13. Ostrach LH, Crabtree JW, Chow K. The ipsilateral retinocollicular projection in the rabbit: an autoradiographic study of postnatal development and effects of unilateral enucleation. J Comp Neurol 1986 254:369– 381.
14. García del Caño G, Gerrikagoitia I, Goñi O, Martínez-Millán L. Sprouting of the visual corticocollicular terminal field after removal of contralateral retinal inputs in neonatal rabbits. Exp Brain Res 1997. 117: 399–410.
15. García del Caño G, Gerrikagoitia I, Martínez-Millán L. Plastic response of the retrospleniocollicular connection after removal of retinal inputs in neonatal rats. Exp Brain Res 2001. 138:343–351.
16. García del Caño G, Gerrikagoitia I, Martínez-Millán L. Plastic reaction of the rat visual corticocollicular connection after contralateral retinal deafferentiation at the neonatal or adult stage: axonal growth vs. reactive synaptogenesis. J Comp Neurol 2002 446:166–178.
17. Gerrikagoitia I, García del Caño G, Martínez-Millán L. Changes of the cholinergic input to the superior colliculus following enucleation in neonatal and adult rats. Brain Res. 2001 898:61–72.
18. Gerrikagoitia I, García del Caño G, Martínez-Millán L. Quantifying presynaptic terminals at the light microscope level in intact and deafferented central nervous structures. Brain Res Protoc 2002 9:165–172.
19. Benedetti F. The development of the somatosensory representation in the superior colliculus of visually deprived mice. Brain Res Dev Brain Res 1992 65:173–178.
20. Mooney RD, Nikoletseas MM, King TD, Savage SV, Weaver MT, Rhoades RW. Structural and functional consequences of neonatal deafferentiation in the superficial layers of the hamster’s superior colliculus. J Comp Neurol 1992. 315:398–412.
21. Mooney RD, Fish SE, Figley BA, Rhoades RW. A transient projection from the trigeminal brainstem complex to the superficial layers of the hamster’s superior colliculus. Exp Brain Res 1991 86:367–372.
22. Huerta MF, Harting JK Tectal control of spinal cord activity: neuroanatomical demonstration of pathways connecting the superior colliculus with the cervical spinal cord grey. Prog Brain Res 1982 57:293–328.
23. Welker C. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 1976 166:173–189.
24. Steiner H, Gerfen CR Tactile sensory input regulates basal and apomorphine-induced immediate-early gene expression in rat barrel cortex. J Comp Neurol 1994 344:297–304.
25. Filipkowski RK, Rydz M, Kaczmarek L Expression of c-Fos, Fos B, Jun B, and Zif268 transcription factor proteins in rat barrel cortex following apomorphine-evoked whisking behavior. Neuroscience 2001 106:679–688.
26. Staiger JF, Bisler S, Schleicher A, et al Exploration of a novel environment leads to the expression of inducible transcription factors in barrel-related columns. Neuroscience 2000 99:7–16.
27. Staiger JF, Masanneck C, Bisler S et al Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment. Neuroscience 2002 109:687–699.
28. Bisler S, Schleicher A, Gass P et al Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-tobarrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment. J Chem Neuroanat 2002 23:187–198.
29. Mana S, Chevalier G Honeycomb-like structure of the intermediate layers of the rat superior colliculus: afferent and efferent connections. Neuroscience 2001 103:673–693.
30. Lee PH, Helms MC, Augustine GJ, Hall WC Role of intrinsic synaptic circuitry in collicular sensorimotor integration. Proc Natl Acad Sci U S A 1997 94:13299–13304.
31. Isa T, Endo T, Saito Y The visuo-motor pathway in the local circuit of the rat superior colliculus. J Neurosci 1998 18:8496–8504.
32. Ozen G, Augustine GJ, Hall WC Contribution of superficial layer neurons to premotor bursts in the superior colliculus. J Neurophysiol 2000 84:460–471.
33. Helms MC, Ozen G, Hall WC Organization of the intermediate gray layer of the superior colliculus. I. Intrinsic vertical connections. J Neurophysiol 2004 91:1706–1715.
34. Perry VH A tectocortical visual pathway in the rat. Neuroscience 1980 5:915–927.
35. Harting JK, Huerta MF, Hashikawa T, van Lieshout DP Projection of the mammlian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J Comp Neurol 1991 304:275–306.
36. Mundiñano IC and Martinez-Millan L Somatosensory cross-modal plasticity in the superior colliculus of the visually deafferented rats. Neuroscience 2010 165:1457-1470.
37. Toldi J, Rojik I, Feher O Neonatal monocular enucleationinduced cross-modal effects observed in the cortex of adult rat. Neuroscience 1994 62:105–114.
38. Volgyi B, Farkas T, Toldi J Compensation of a sensory deficit inflicted upon newborn and adult animals. A behavioural study. Neuroreport 1993 4:827–829.