Abstract
Lesions of the superior colliculus in rats attenuate the oral stereotypy produced by systemic administration of dopamine agonists. Current evidence suggests that such drugs affect the superior colliculus by reducing transmission in the inhibitory GABAergic nigrotectal pathway. To investigate whether the superior colliculus plays a direct role in producing stereotyped oral movements, the present experiment therefore examined the effects of collicular microinjections of the GABA antagonist picrotoxin on the behaviour of rats observed in an open-field.
Gnawing was observed after injections of picrotoxin (25 ng) into sites in the intermediate and deep layers of the superior colliculus, consistent with the superior colliculus playing a direct part in producing the stereotyped gnawing seen after systemic administration of dopamine agonists. However, gnawing was only observed after a period in which the animal showed strong avoidance reactions, to stimuli that normally evoked orienting or little reaction. This change in reactivity was observed after injections of picrotoxin into all parts of the colliculus, but the most sensitive (responding to doses as low as 12.5 ng) were mainly in the superficial and intermediate layers. It appears that there may be more than one GABAergic system within the superior colliculus.
Similar content being viewed by others
References
Baldessarini RJ, Tarsy D (1980) Dopamine and the pathophysiology of dyskinesias induced by antipsychotic drugs. Ann Rev Neurosci 3:23–41
Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191–217
Blair, R, Livan J, Cytryniak H, Shizgal P, Amit Z (1978) Explosive motor behavior, rigidity and periaqueductal gray lesions. Neuropharmacology 17:205–209
Brown LL, Wolfson LI (1978) Apomorphine increases glucose utilization in the substantia nigra, subthalamic nucleus and corpus striatum of rat. Brain Res 140:188–193
Clavier RM, Atmadja S, Fibiger HC (1976) Nigrothalamic projections in the rat as demonstraed by orthograde and retrograde tracing techniques. Brain Res Bull 1:379–384
Dean P, Redgrave P, Pope SG (1979) Effects of superior-colliculus lesions on apomorphine-induced activity and stereotypy in rats. Soc Neurosci Abstr 5:332
Dean P, Redgrave P, Souki W, Lewis G (1980) Behavioural effects of microinjections of picrotoxin into rat superior colliculus, and their modulation by intranigral 6-OHDA. Br J Pharmacol 70:P145
Deniau JM, Hammond-Le Guyader C, Feger J, McKenzie JS (1977) Bilateral projection of nigrocollicular neurons: An electrophysiological analysis in the rat. Neurosci Lett 5:45–50
Di Chiara G, Porceddu ML, Morelli M, Mulas ML, Gessa GL (1978) Strio-nigral and nigro-thalamic GABA-ergic neurons as output pathways for striatal responses. In: GABA-neurotransmitters, Krogsgaard-Larsen P, Scheel-Krüger J, Kofod E (eds) Munksgaard, Copenhagen, pp 464–481
Di Chiara G, Morelli M Porceddu ML, Gessa GL (1979a) Role of thalamic gamma-aminobutyrate in motor functions: catalepsy and ipsiversive turning after intrathalamic muscimol. Neuroscience 4:1453–1465
Di Chiara G, Porceddu ML, Morelli M, Mulas ML, Gessa GL (1979b) Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res 176:273–284
Faull RLM, Mehler WR (1978) The cells of origin of nigrotectal, nigrothalamic and nigrotriatal projections in the rat. Neuroscience 3:989–1002
Foreman NF, Goodale MA, Milner AD (1978) Nature of postoperative hyperactivity following lesions of the superior colliculus in the rat. Physiol Behav 21:157–160
Hopkins DA, Niessen LW (1976) Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey. Neurosci. Lett 2:253–259
Kawai N, Yamamoto C (1967) Effects of gamma-aminobutyric acid on the potentials evoked in vitro in the superior colliculus. Experientia 23:822–823
McCulloch J, Savaki HE, McCulloch MC, Sokoloff L (1980) Retina-dependent activation by apomorphine of metabolic activity in the superficial layer of the superior colliculus. Science 207:313–315
Morelli M, Porceddu ML, Di Chiara G (1980) Lesions of substantia nigra by kainic acid: effects on apomorphine-induced stereotyped behaviour. Brain Res 191:67–78
Okada Y (1974) Distribution of gamma-aminobutyric acid (GABA) in the layers of superior colliculus of the rabbit. Brain Res 75:362–365
Olds J, Peretz B (1960) A motivational analysis of the reticular activating system. Electroencephalogr Clin Neurophysiol 12:445–454
Olianas MC, De Montis GM, Concu A, Tagliamonte A, Di Chiara G (1978) Intranigral kainic acid: evidence for nigral, non-dopaminergic neurons controlling posture and behavior in a manner opposite to the dopaminergic ones. Eur J Pharmacol 49:223–232
Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A stereotaxic atlas of the rat brain, 2nd edn. Plenum Press, New York
Pope SG, Dean P (1979) Hyperactivity, aphagia and motor disturbance following lesions of superior colliculus and underlying tegmentum in rats. Behav Neural Biol 27:433–453
Pope SG, Dean P, Redgrave P (1980) Dissociation of d-amphetamine-induced locomotor activity and stereotyped behaviour by lesions of the superior colliculus. Psychopharmacology 70:297–302
Redgrave P, Dean P, Donohoe TP, Pope SG (1980) Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotype: a possible role for the nigrotectal pathway. Brain Res 196:541–546
Schaeffer KP (1970) Unit analysis and electrical stimulation in the optic tectum of rabbits and cats. Brain Behav Evol 3:222–240
Scheel-Krüger J, Arnt J, Magelund G (1977) Behavioural stimulation induced by muscimol and other GABA agonists injected into the substantia nigra. Neurosci Lett 1:351–356
Sherk H (1979) Connections and visual-field mapping in cat's tectopara-bigeminal circuit. J Neurophysiol 42:1656–1668
Sterling P, Spencer RF (1976) Autoradiographic identification of neurons that accumulate tritiated GABA in the cat superior colliculus. Neurosci Abstr 2:1095
Vincent SR, Hattori T, McGeer EG (1978) The nigrotectal projection: a biochemical and ultrastructural characterization. Brain Res 151:159–164
Waldbillig RJ (1975) Attack, eating, drinking and gnawing elicited by electrical stimulation of rat mesencephalon, and pons. J Comp Physiol Psychol 89:200–212
Wright AK, Arbuthnott GW (1980) Non-dopamine containing effecents of substantia nigra: the pathway to the lower brain stem. J Neural Transm 47:221–226
Yamashita J, Hirata Y (1978) Running fits induced by direct administration of semicarbazide into the superior colliculus of the mouse. Neurosci Lett 8:89–92
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Redgrave, P., Dean, P., Souki, W. et al. Gnawing and changes in reactivity produced by microinjections of picrotoxin into the superior colliculus of rats. Psychopharmacology 75, 198–203 (1981). https://doi.org/10.1007/BF00432187
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00432187