Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway

Redgrave, Peter; Dean, Paul; Donohoe, Thomas P.; Pope, Sian G.

doi:10.1016/0006-8993(80)90422-9

Cited by 79 publications

(16 citation statements)

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“…This finding is consistent with a number of studies showing a reduction in dopamine agonist-stimulated behaviors after lesions of the deep SC Redgrave et al, 1980;Morelli et al, 1981;Kilpatrick et al, 1982) Because blockade of GABA transmission in the deep SC/Me elicits motor behaviors resembling those seen after the administration of dopamine agonists, including an enhancement of startle (present study), we addressed the possibility that removal of GABA tone at this level may mediate the enhancement of startle by SKF 82958. This hypothesis is supported by the observation that GABA levels in the deep SC are reduced after systemic administration of dopamine agonists (Melis and Gale, 1983).…”

Section: Muscimol In the Deep Sc/me And The Enhancement Of Startle Bysupporting

confidence: 91%

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats

Meloni

Davis

2000

J. Neurosci.

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GABA transmission in the deep layers of the superior colliculus/ deep mesencephalic reticular formation (deep SC/Me) mediates several motor responses, including those expressed after systemic administration of dopamine agonists. In the present study we examined the role of the deep SC/Me in the modulation of the acoustic startle reflex and its enhancement by the dopamine D 1 agonist SKF 82958. Rats were implanted with bilateral cannulas into the deep SC/Me or superficial layers of the SC (super SC) and 1 week later were infused with various compounds. The GABA A antagonist bicuculline (0, 5, and 10 ng) produced a doseand time-dependent enhancement of startle after infusion into the deep SC/Me, but not the super SC. Infusion of the GABA A agonist muscimol (0.1 g) into the deep SC/Me, but not the super SC, blocked the enhancement of startle by systemic SKF 82958 (1 mg/kg) but had no effect on baseline startle by itself. This effect was not produced by infusion of the D 1 antagonist SCH 23390(1 g) or the glutamate antagonist NBQX (0.1 g). Deposits of FluoroGold into the deep SC/Me, combined with immunohistochemistry for glutamic acid decarboxylase (GAD), confirmed a direct GABAergic input from the substantia nigra pars reticulata (SNr) to the deep SC/Me. These results suggest that GABA tone in the deep SC/Me modulates the expression of startle as well as the enhancement of startle by dopamine D 1 agonists. On the basis of these data and previous work, we have proposed a striatonigral-tectal-reticular neural pathway mediating the effects of dopamine D 1 agonists on startle. Key words: startle; superior colliculus; bicuculline; muscimol; SKF 82958; D 1 receptorThe acoustic startle reflex in rats is a rapid sensorimotor response elicited by a sudden and intense auditory stimulus (cf. Davis, 1984) and is mediated by a simple neural pathway in the brainstem consisting of cochlear root neurons (CRNs), neurons in the nucleus reticularis pontis caudalis (PnC), and motoneurons in the spinal cord (Lee et al., 1996). The amplitude of this short-latency response can be quantified easily and has been used extensively to study the neurocircuitry and neurochemistry involved in the modulation of reflex/motor behavior (cf. Davis, 1980). Along these lines, we have found that systemic administration of dopamine D 1 receptor agonists markedly increases the acoustic startle response (Meloni and Davis, 1999a). This effect is mediated in part by the activation of D 1 receptors in the substantia nigra pars reticulata (SNr; Meloni and Davis, 1997), a major output structure of the basal ganglia to premotor areas in the midbrain (Graybiel, 1984). Hence, we have been using D 1 agonist-induced enhancement of the acoustic startle response to study the neural mechanisms underlying dopaminergic control of motor behavior. In particular, we are interested in how SNr-dependent D 1 receptor agonist effects get transmitted to the primary acoustic startle pathway in the brainstem.In the present study we have focused on the deep layers of the superior c...

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Section: Muscimol In the Deep Sc/me And The Enhancement Of Startle Bysupporting

confidence: 91%

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats

Meloni

Davis

2000

J. Neurosci.

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“…Indeed, extending the range of dopamine's functions to include its direct, GABA-attenuating effects may help to resolve certain discrepancies that have already developed in the literature with regard to the net effect of dopamine on basal ganglia output transmission. For instance, it is widely believed that activation of striatal dopamine receptors, as produced by systemic administration of drugs like apomorphine, causes an inhibition of substantia nigra output function, presumably mediated by activation of striatonigral GABAergic pathways to reticulata neurons (Childs and Gale, 1983;DiChiara et al, 1978;Kilpatrick et al, 1982;Olianas et al, 1978;Reavill et al, 198 1;Redgrave et al, 1980;Scheel-Kruger, 1982). However, singleunit recording studies of the effects of i.v.…”

Section: Discussionmentioning

confidence: 99%

Endogenous dopamine can modulate inhibition of substantia nigra pars reticulata neurons elicited by GABA iontophoresis or striatal stimulation

Waszczak¹,

Walters²

1986

J. Neurosci.

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Previous reports from this laboratory have described an ability of iontophoretically applied dopamine to attenuate the inhibitory effects of iontophoresed GABA on neurons of the substantia nigra pars reticulata. This finding raised the question of whether endogenous dopamine, released from dendrites of neighboring pars compacta dopamine neurons, might act as a neuromodulator which diminishes the inhibition of pars reticulata neurons evoked by either GABA iontophoresis or electrical stimulation of the striatonigral GABAergic pathway. Extracellular, single-unit activity of pars reticulata neurons was recorded in male rats anesthetized with chloral hydrate. In one set of studies, d-amphetamine, a drug reported to release dopamine from nigral dendrites, was administered intravenously (1.6 mg/kg) during regular, intermittent iontophoretic pulses of GABA. As had been previously observed with iontophoresed dopamine, i.v. amphetamine significantly lessened the inhibition of reticulata neurons produced by GABA application. This change was reflected by a decrease in GABA's inhibitory potency by 22% relative to the control level of inhibition achieved prior to amphetamine administration. Amphetamine caused no decreases in GABA's effectiveness, however, in animals that had previously received treatments that depleted or destroyed nigral dopamine stores, i.e., in rats pretreated with reserpine and alpha- methyl-p-tyrosine, or in rats with 6-hydroxydopamine lesions of the nigrostriatal dopamine pathway. In a second set of experiments, amphetamine or dopamine was delivered iontophoretically while monitoring the GABA-mediated (bicuculline-reversible) inhibition of reticulata neurons that can be elicited by striatal stimulation.(ABSTRACT TRUNCATED AT 250 WORDS)

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“…Recent studies have indicated that the stereotyped behaviour induced in rats by dopamine agonists such as apomorphine can be attenuated by bilateral, extensive, lesions of superior colliculus, and it has been suggested that dopamine related oral stereotypies may reflect release of colliculus mechanisms from nigrally mediated (GABA-ergic) inhibitory control (Redgrave et aL, 1980).…”

Section: Nigro-tectal and Tecto-spinal Pathwaysmentioning

confidence: 99%

Basal ganglia outflow pathways and circling behaviour in the rat

Leigh

Reavill

Jenner

et al. 1983

J. Neural Transmission

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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 apomorphine-induced 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 gigantocellularis 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.(ABSTRACT TRUNCATED AT 400 WORDS)

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Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway

Cited by 79 publications

References 15 publications

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats

Endogenous dopamine can modulate inhibition of substantia nigra pars reticulata neurons elicited by GABA iontophoresis or striatal stimulation

Basal ganglia outflow pathways and circling behaviour in the rat

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Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway

Cited by 79 publications

References 15 publications

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D1Receptor Agonist SKF 82958 in Rats

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D1Receptor Agonist SKF 82958 in Rats

Endogenous dopamine can modulate inhibition of substantia nigra pars reticulata neurons elicited by GABA iontophoresis or striatal stimulation

Basal ganglia outflow pathways and circling behaviour in the rat

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GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D₁Receptor Agonist SKF 82958 in Rats