Summary
The role of efferents in substantia nigra pars reticulata in the mediation of circling behaviour in the rat has been studied by means of lesions designed to interrupt these pathways or to damage nigral projection areas. The behavioural model used was the circling rodent with a prior 6-hydroxydopamine lesion of the left nigro-striatal pathway in which amphetamine induced ipsiversive rotation and apomorphine induced contraversive rotation.
Removal of the left fronto-parietal cortex caused only a transient decrease in drug-induced rotation. An electrolytic lesion of the left, right or both parafascicular thalamic nuclei did not alter circling behaviour. Electrolytic lesioning of the left ventromedial thalamus decreased apomorphineinduced contraversive circling whereas a lesion of the right ventromedial thalamus decreased amphetamine-induced ipsiversive rotation. Bilateral electrolytic lesions of the ventromedial thalamus did not alter drug-induced circling.
Unilateral or bilateral electrolytic lesioning of the medial superior colliculus did not alter the rotational response to apomorphine or amphetamine. However, an electrolytic lesion interrupting the dorsal tegmental decussation reduced apomorphine-induced circling but not amphetamine-induced circling.
That a critical role for the nigro-thalamic and nigro-tectal pathways is not involved in the mediation of circling behaviour was confirmed by placing knife cuts so as to separate these structures from the substantia nigra; such lesions failed to alter the contraversive rotation induced by the ipsilateral injection of muscimol into substantia nigra pars reticulata.
Electrolytic lesions of the ipsilateral nucleus reticularis gigantocellu laris or kainic acid lesions of the ipsilateral nucleus tegmenti pedunculopontinus did not alter drug-induced circling in animals with a prior 6-hydroxydopamine nigral lesion. In contrast, an ipsilateral lesion of the midbrain periaqueductal grey matter and adjacent midbrain reticular formation (the angular complex) decreased apomorphine-induced contraversive rotation in such animals, while bilateral lesions reduced both apomorphine-and amphetamine-induced circling; in each case the postural component of rotation was abolished.
Unilateral kainic acid lesions of the angular complex in naive animals caused ipsiversive rotation which was enhanced by apomorphine. Unilateral kainic acid lesions of the angular complex with an ipsilateral 6-hydroxydopamine nigral lesion caused reversal of the previous contraversive rotation to apomorphine, and enhanced amphetamine-induced ipsiversive rotation.
A nigro-reticular pathway to the midbrain reticular formation adjacent to the periaqueductal grey matter (the angular complex) appears critical in the mediation of the postural component of drug-induced rotation in animals with a prior unilateral 6-hydroxydopamine lesion of the dopaminergic nigro-striatal system. Nigro-thalamic pathways and pathways from nigra to the superficial and medial superior colliculus do not seem to be involved, although we cannot exclude a role for the deep lateral superior colliculus which, in any case, is anatomically and functionally closely related to the midbrain tegmental reticular formation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahlenius, S.: Potentiation by haloperidol of the catalepsy produced by lesions in the parafascicular nucleus in the rat. Brain Res.150, 648–652 (1978).
Beckstead, R. M., Domesick, V. B., Nauta, W. J. H.: Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res.175, 191–217 (1979).
Bentivoglio, M., Van Der Kooy, D., Kuypers, H. G. J. M.: The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labelling study. Brain Res.174, 1–17 (1979).
Brownstein, M. J., Mroz, E. A., Kizer, J. S., Palkovits, M., Leeman, S.: Regional distribution of substance P in the brain of the rat. Brain Res.116, 299–305 (1976).
Brodal, A.: The reticular formation of the brainstem. Anatomical aspects and functional correlations. Edinburgh-London: Oliver & Boyd. 1957.
Castaldi, L.: Studi sulla struttura a sullo svielluppo del mesencefala. Ricerche in Cavia cobaya. Arch. Ital. Anat. Embriol.20, 223–225 (1923).
Castiglioni, A. J., Gallaway, M. C., Coutter, J. D.: Spinal projections from the midbrain in the monkey. J. Comp. Neurol.178, 329–346 (1978).
Clavier, R. M., Atmadja, S., Fibiger, H. C.: Nigrothalamic projections in the rat as demonstrated by orthograde and retrograde tracing techniques. Brain Res. Bull.1, 379–384 (1976).
Commissiong, J. W., Gentleman, S., Neff, N. H.: Spinal cord dopaminergic neurones: evidence of an uncrossed nigrospinal pathway. Neuropharmacol.18, 565–568 (1979).
Crossman, A. R., Sambrook, M. A., Gergies, S. W., Slater, P.: The neurological basis of motor asymmetry following unilateral 6-hydroxydopamine brain lesions in the rat: the effect of motor decortication. J. Neurol. Sci.34, 407–414 (1977).
Crossman, A. R., Sambrook, M. A.: The neurological basis of motor asymmetry following unilateral nigrostriatal lesions in the rat: the effect of secondary superior colliculus lesions. Brain Res.159, 211–213 (1978).
De Groot, J.: The rat brain in stereotaxic coordinates. Verh. Kon. Ned. Akad. Wet.51, 11–40 (1959).
Denny-Brown, D.: The midbrain and motor integration. Proc. Royal Soc. Med.55, 527–538 (1962).
Di Chiara, G., Porceddu, M. L., Morelli, M., Mulas, M. L., Gessa, G. G.: Substantia nigra as an output station for striatal dopaminergic responses: role of GABA-mediated inhibition of pars reticulata neurons. Naunyn-Schmied. Arch. Pharmac.306, 153–159 (1979 a).
Di Chiara, G., Morelli, M., Porceddu, M. L., Gessa, G. L.: Role of thalamicγ-aminobutyrate in motor functions: catalepsy and ipsiversive turning after intrathalamic muscimol. Neuroscience4, 1453–1465 (1979 b).
Di Chiara, G., Morelli, M., Imperato, A., Porceddu, M. L.: A re-evaluation of the superior colliculus in turning behaviour. Brain Res.237, 61–77 (1982).
Donaldson, I. MacG., Dolphin, A. C., Jenner, P., Marsden, C. D., Pycock, C.: The involvement of noradrenaline in motor activity as shown by rotational behaviour after unilateral lesions of the locus coeruleus. Brain99, 417–446 (1976).
Donaldson, I. MacG., Pycock, C., Marsden, C. D.: Rotation produced by electrolytic lesions of the superior cerebellar peduncle in rats modifying other forms of circling behaviour. Exp. Neurol.52, 119–131 (1976).
Donaldson, I. MacG., Dolphin, A. C., Jenner, P., Pycock, C., Marsden, C. D.: Rotational behaviour produced in rats by unilateral electrolytic lesions of the ascending noradrenergic bundles. Brain Res.138, 487–509.
Earley, C. J., Leonard, B. E.: Isolation and assay of noradrenaline, dopamine, 5-hydroxytryptamine, and several metabolites from brain tissue using disposable Bio-Rad columns packed with Sephadex G-10. J. Neuropharmac. Methods1, 67–79 (1978).
Elde, R. P., Hokfelt, T., Johansson, O., Terenius, L.: Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience1, 349–351 (1976).
Garcia-Munoz, M., Nicolaou, N. M., Tulloch, I. F., Wright, A. K., Arbuthnott, G. W.: Feedback loop or output pathway in striato-nigral fibres. Nature (Lond.)265, 363–365 (1977).
Garcia-Munoz, M., Patino, P., Chavez, L.: Substantia nigra reticulata efferents involved in turning behaviour. Neurosci. Lett. Suppl.7, 5314 (1981).
Garcia-Munoz, M., Patino, P., Wright, M. J., Arbuthnott, G. W.: The anatomical substrate of the turning behaviour seen after lesions in the nigrostriatal dopamine system. Neuroscience8, 87–95 (1983).
Garcia-Munoz, M., Patino, P., Aguilar, R., Arbuthnott, G.: Participation of projections from substantia nigra reticulata to the lower brain stem in turning behaviour. Exp. Neurol.78, 380–390 (1982).
Graybiel, A. M., Sciascia, T. R.: Origin and distribution of nigrotectal fibres in the cat. Neuroscience Abstracts1, 174 (1975).
Grofova, I., Ottersen, O. P., Rinvik, E.: Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal grey substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Res.146, 205–220 (1978).
Hedreen, J. C.: Separate demonstration of dopaminergic and non-dopaminergic projections of the substantia nigra of the rat. Anat. Rec.169, 338, (1971).
Herkenham, M.: The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J. Comp. Neurol.183, 487–518 (1979).
Hopkins, D. A., Niessen, L. W.: Substantia nigra projections to the reticular formation, superior colliculus and central grey in the rat, cat, and monkey. Neurosci. Lett.2, 253–259 (1976).
Jackson, A., Crossman, A. R.: Basal ganglia and other afferent projections to the peribrachial region in the rat: a study using retrograde and anterograde transport of horseradish peroxidase. Neuroscience6, 1537–1549 (1981a).
Jackson, A., Crossman, A. R.: Subthalamic projection to nucleus tegmenti pedunculopontinus in rat. Neurosci. Lett.22, 17–22 (1981 b).
James, T. A., Starr, M. S.: The role of GABA in the substantia nigra. Nature (Lond.)275, 229–230 (1978).
Jaquet, Y. F., Carol, M., Russell, I. S.: Morphine-induced rotation in naive, non-lesioned rats. Science192, 261–263 (1976).
Jenner, P., Leigh, N., Marsden, C. D., Reavill, C.: Involvement of the periaqueductal grey in dopamine mediated circling behaviour. Br. J. Pharmac.72, 492 P (1981).
Kelly, P. H., Moore, K. E.: Mesolimbic dopaminergic neurones in the rotational model of nigrostriatal function. Nature (Lond.)263, 695–696 (1976).
Kilpatrick, I. C., Collingridge, G. L., Starr, M. S.: Evidence for the participation of nigrotectalγ-aminobutyrate neurones in striatal- and nigral-derived circling in the rat. Neuroscience7, 207–222 (1982).
Kilpatrick, I. C., Starr, M. S.: The nucleus tegmenti pedunculopontinus and circling behaviour in the rat. Neurosci. Lett.26, 11–16 (1978).
Kilpatrick, I. C., Starr, M. S., Fletcher, A., James, T. A., Macleod, N. K.: Evidence for a GABA-ergic nigrothalamic pathway in the rat. I. Behavioural and biochemical studies. Exp. Brain Res.40, 45–54 (1980).
Konig, J. F. R., Klippel, R.: The rat brain. A stereotaxic atlas of the forebrain and lower part of the brainstem. Baltimore: Williams & Wilkins. 1963.
Krieg, W. J. S.: Accurate placement of minute lesions in the brain of the albino rat. Quart. Bull. Northwestern Univ. Med. School20, 199–208 (1946).
Laverty, R., Sharman, D. F.: The estimation of small quantities of 3,4-dihydroxyphenylethylamine in tissues. Br. J. Pharmac.24, 538–548 (1965).
Lee, L. A., Crossman, A. R., Slater, P.: The neurological basis of striatally induced head-turning in the rat: the effects of lesions in putative output pathways. Neuroscience5, 73–79 (1980).
Leviel, V., Cheramy, A., Nieoullon, A., Glowinski, J.: Symmetrical bilateral changes in dopamine release from the caudate nuclei of the cat induced by unilateral nigral application of glycine and GABA-related compounds. Brain Res.75, 259–270 (1979).
Maickel, R. P., Cox, R. H. jr., Saillant, J., Miller, F. P.: A method for the determination of serotonin and norepinephrine in discrete areas of rat brain. Int. J. Neuropharmac.7, 275–281 (1968).
Marshall, J. F., Turner, B. H., Teitelbaum, P.: Sensory neglect produced by lateral hypothalamic damage. Science174, 523–525 (1971).
Marshall, J. F., Ungerstedt, U.: Striatal efferent fibers play a role in maintaining rotational behaviour in the rat. Science198, 62–64 (1977).
Martin, G. F., Humbertson, A. O., Laxson, L. C., Pannetou, W. M., Tschismadia, I.: Spinal projections from the mesencephalic and pontine reticular formation in the North American opossum: a study using axonal transport techniques. J. Comp. Neurol.187, 373–400 (1979).
Mason, S. T., Fibiger, H. C.: On the specificity of kainic acid. Science204, 1339–1341 (1979).
Miller, C. A., Sinnamon, H. M.: Excitatory projections between the midbrain tegmental area and the pontine reticular formation of the rat. Brain Res.191, 533–537 (1980).
Morelli, M., Imperato, A., Porceddu, M. L., Di Chiara, G.: Role of the dorsal mesencephalic reticular formation and deep layers of superior colliculus in turning behaviour elicited from the striatum. Brain Res.215, 337–341 (1981).
Motamedi, F., York, D. H.: A descending pathway involving nigral-induced head turning movements. Neurosci. Abstr.4, 47 (1978).
Mulas, A., Longoni, R., Spina, L., Del Fiacco, M., Di Chiara, G.: Ipsiversive turning behaviour after discrete unilateral lesions of the dorsal mesencephalic reticular formation by kainic acid. Brain Res.208, 468–472 (1981).
Nauta, H. J. W.: A proposed conceptual reorganisation of the basal ganglia and telencephalon. Neuroscience4, 1875–1881 (1979).
Nauta, H. J. W., Cole, M.: Efferent projections of the subthalamic nucleus: an autoradiographic study in monkey and cat. J. Comp. Neurol.180, 1–16 (1978).
Nauta, W. J. H., Mehler, W. R.: Projections of the lentiform nucleus in the monkey. Brain Res.1, 3–41 (1966).
Nyberg-Hansen, R.: The location and termination of tectospinal fibres in the cat. Exp. Neurol.9, 212–227 (1964).
Olianas, M. C., De Montis, G. M., Concu, A., Tagliamonte, A., Di Chiara, G.: Intranigral kainic acid: evidence for nigral non-dopaminergic neurons controlling posture and behaviour in a manner opposite to the dopaminergic ones. Eur. J. Pharmac.49, 223–232 (1978).
Orlovski, G. N.: Connexions of the reticulospinal neurones with the “locomotor sections” of the brainstem. Biophysics15, 761–771 (1970).
Pellegrino, L. J., Cushman, A. J.: A stereotaxic atlas of the rat brain. New York: Meredith. 1971.
Peterson, B. W., Pitts, N. G., Fukushima, K.: Reticulospinal connections with limb and axial motoneurons. Exp. Brain Res.36, 1–20 (1979).
Petrovicky, P.: Projections from the tectum mesencephali to the brainstem structures in the rat. Fol. Morph.24, 41–48 (1976).
Pycock, C. J., Marsden, C. D.: The rotating rodent: a two component system? Eur. J. Pharmac.476, 167–175 (1978).
Reavill, C., Jenner, P., Leigh, N., Marsden, C. D.: Turning behaviour induced by injection of muscimol or picrotoxin into the substantia nigra demonstrates dual GABA components. Neurosci. Lett.12, 323–328 (1979 a).
Reavill, C., Leigh, N., Jenner, P., Marsden, C. D.: Dopamine mediated circling behaviour does not involve the nigro-tectal pathway. Exp. Brain Res.37, 309–316 (1979 b).
Reavill, C., Jenner, P., Leigh, N., Marsden, C. D.: The role of nigral projections to the thalamus in drug-induced circling behaviour in the rat. Life Sci.28, 1457–1466 (1981).
Redgrave, P., Dean, P., Donohoe, T. P., Pope, S. G.: Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway. Brain Res.196, 541–546 (1980).
Royce, G. J.: Cells of origin of subcortical afferents to the caudate nucleus: a horseradish peroxidase study in the cat. Brain Res.153, 465–475 (1978).
Scheel-Kruger, J., Arnt, J., Magelund, G.: Behavioural stimulation induced by muscimol and other GABA agonists injected into the substantia nigra. Neurosci. Lett.4, 351–356 (1977).
Schwarz, R., Coyle, J. T.: Neurochemical sequelae of kainate injections in corpus striatum and substantia nigra of the rat. Life Sci.20, 431–436 (1977).
Sprague, J. M., Meikle, T. H.: The role of the superior colliculus in visually guided behaviour. Exp. Neurol.11, 115–146 (1965).
Taber, E.: The cytoarchitecture of the brainstem of the cat. I. Brainstem nuclei of the cat. J. Comp. Neurol.116, 27–69 (1961).
Tohyama, M., Sakai, K., Salvert, D., Touret, M., Jouvet, M.: Spinal projections from the lower brainstem in the cat as demonstrated by the horseradish peroxidase technique. I. Origins of the reticulo-spinal tracts and their funicular trajectories. Brain Res.173, 383–403 (1979).
Ungerstedt, U.: Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol. Scand., Suppl.367, 1–48 (1971a).
Ungerstedt, U.: Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. Acta Physiol. Scand., Suppl.367, 49–68 (1971b).
Ungerstedt, U.: Postsynaptic supersensitivity after 6-hydroxydopamine induced degeneration of the nigrostriatal dopamine systems. Acta Physiol. Scand., Suppl.367, 69–93 (1971 c).
Valverde, F.: Reticular formation of the albino rats brainstem. Cytoarchitecture and corticofugal connections. J. Comp. Neurol.119, 25–53 (1980).
Winterkorn, J. M. S., Meikle, J. H.: Lesions of the tectospinal tract do not produce compulsive circling. Brain Res.190, 597–600 (1980).
Wirtshafter, D., Asin, K. E., Kent, E. W.: Role of the tectospinal tract in apomorphine induced rotation. Neurosci. Abstr.4, 287 (1978).
York, D. H., Faber, J. E.: An electrophysiological study of nigrotectal relationships: a possible role in turning behaviour. Brain Res.130, 383–386 (1977).
Zemlan, F. P., Pfaff, D. W.: Topographical organization in medullary reticulospinal systems as demonstrated by horseradish peroxidase technique. Brain Res.174, 161–166 (1979).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Leigh, P.N., Reavill, C., Jenner, P. et al. Basal ganglia outflow pathways and circling behaviour in the rat. J. Neural Transmission 58, 1–41 (1983). https://doi.org/10.1007/BF01249122
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01249122