Skip to main content

Enhanced GABA function in the angular complex (lateral periaqueductal grey matter and adjacent reticular formation) alters the postural component of striatal- or nigral-derived circling

Experimental Brain Research volume 56, pages 1–11 (1984)Cite this article

Summary

Unilateral injection of muscimol into the angular complex (lateral periaqueductal grey matter and adjacent reticular formation) caused ipsiversive rotation. Focal injection of picrotoxin into the same site produced contraversive rotation. Administration of apomorphine to animals with a unilateral 6OHDA lesion of the left medial forebrain bundle caused contraversive rotation. Focal injection of muscimol into the angular complex reversed the direction of rotation such that apomorphine administration now produced ipsiversive circling. Unilateral injection of muscimol into substantia nigra zona reticulata caused contraversive rotation. Focal injection of picrotoxin into the same site produced ipsiversive rotation. The prior injection of muscimol into the ipsilateral angular complex prevented the contraversive rotation induced by intranigral administration of muscimol such that animals now showed ipsiversive circling. In both 6-OHDA-lesioned animals and animals receiving intranigral muscimol, focal injection of muscimol into the angular complex caused a reversal in the direction of circling through loss of the postural component with no obvious change in locomotor activity. Bilateral electrolytic lesions of the angular complex overall had no effect on amphetamine-induced locomotion. Manipulation of GABA function in the angular complex alters circling behaviour initiated from the striatum or substantia nigra by altering the postural component without affecting the locomotor response of the animals. The data suggest a critical role for the angular complex as an outflow station from basal ganglia.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Ahlenius S (1978) Potentiation by haloperidol of the catalepsy produced by lesions in the parafascicular nucleus in the rat. Brain Res 150: 648–652

    Google Scholar 

  • Anderson M, Yoshida M (1977) Electrophysiological evidence for branching nigral projections to the thalamus and superior colliculus. Brain Res 137: 361–364

    Google Scholar 

  • Basbaum AI, Fields HL (1978) The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J Comp Neurol 187: 513–532

    Google Scholar 

  • Beckstead RM, Domesick VB, Nauta WH (1979) The organization of the efferent projections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175: 191–217

    Google Scholar 

  • Bentivoglio M, Van Der Kooy D, Kuypers HGJM (1979) The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labelling study. Brain Res 174: 1–17

    Google Scholar 

  • Childs JA, Gale K (1983) Neurochemical evidence for a nigrotegmental GABAergic projection. Brain Res 258: 109–114

    Google Scholar 

  • Clavier RM, Atmadja S, Fibiger HC (1976) Nigrothalamic projections in the rat as demonstrated by orthograde and retrograde tracing techniques. Brain Res Bull 1: 379–384

    Google Scholar 

  • Crossman AR, Sambrook MA (1978) 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

    Google Scholar 

  • Dean P, Redgrave P, Eastwood L (1982a) Suppression of apomorphine-induced oral stereotypy in rats by microinjection of muscimol into midbrain. Life Sci 30: 2171–2180

    Google Scholar 

  • Dean P, Redgrave P, Lewis G (1982b) Locomotor activity of rats in open field after microinjection of procaine into superior colliculus or underlying reticular formation. Behav Brain Res 5: 175–188

    Google Scholar 

  • De Groot J (1967) The rat brain in stereotaxic coordinates. Vehr Kon Ned Akad Wet 52: 11–40

    Google Scholar 

  • Di Chiara G, Porceddu ML, Morelli M, Mulas ML, Gessa GL (1979a) 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

    Google Scholar 

  • Di Chiara G, Porceddu ML, Morelli M, Gessa GL (1979b) Substantia nigra as an output station for striatal dopaminergic responses: role of GABA-mediated inhibition of pars reticulata neurons. Naunyn-Schmied Arch Pharmacol 306: 153–159

    Google Scholar 

  • Di Chiara G, Morelli M, Imperato A, Porceddu ML (1982) A reevaluation of the role of the superior colliculus in turning behaviour. Brain Res 237: 61–77

    Google Scholar 

  • Edwards SB (1980) The deep layers of the superior colliculus: their reticular characteristics and structural organization. In: Hobson, Brazier (eds) The reticular formation revisited. Raven Press, New York

    Google Scholar 

  • Garcia-Munoz M, Nicolaou NM, Tulloch IF, Wright AK, Arbuthnott G (1977) Feedback loop or output pathway in striatonigral fibres. Nature 265: 363–365

    Google Scholar 

  • Garcia-Munoz M, Patino P, Aguilar R, Arbuthnott G (1982) Participation of projections from substantia nigra reticulata to the lower brain stem in turning behaviour. Exp Neurol 78: 380–390

    Google Scholar 

  • Gerfen CR, Staines WA, Arbuthnott GW, Fibiger MC (1982) Crossed connections of the substantia nigra in the rat. J Comp Neurol 207: 283–303

    Google Scholar 

  • Graybiel AM, Sciascia TR (1975) Origin and distribution of nigrotectal fibres in the cat. Neurosci Abstr 1: 56

    Google Scholar 

  • Grofova I, Ottersen OP, Rinvik E (1978) 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

    Google Scholar 

  • Hedreen JC (1971) Separate demonstration of dopaminergic and non-dopaminergic projections to the substantia nigra of the rat. Anat Rec 169: 338

    Google Scholar 

  • Herkenham M (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol 183: 487–518

    Google Scholar 

  • Hopkins DA, Niessen LW (1976) Substantia nigra projections to the reticular formation, superior colliculus and central grey in the rat, cat and monkey. Neurosci Lett 2: 253–259

    Google Scholar 

  • Huerta MF, Harting JK (1982) Projections of the superior colliculus to the supraspinal nucleus and the cervical spinal cord gray of the cat. Brain Res 242: 326–331

    Google Scholar 

  • Imperato A, Di Chiara G (1981) Behavioural effects of GABAagonists and antagonists infused in the mesencephalic reticular formation-deep layers of the superior colliculus. Brain Res 224: 185–194

    Google Scholar 

  • James TA, Starr MS (1978) The role of GABA in the substantia nigra. Nature 275: 229–230

    Google Scholar 

  • Jenner P, Leigh N, Marsden CD, Reavill C (1981) Involvement of the periaqueductal grey in dopamine mediated circling behaviour. Br J Pharmacol 72: 492p

  • Jenner P, Leigh N, Marden CD, Muscatt S, Reavill C (1982) Modulation of GABA function in the angular complex mimics dopamine-mediated circling behaviour. Br J Pharmacol 75: 85p

  • Kelly PH, Moore KE (1976) Mesolimbic dopamine neurones in the rotational model of nigrostriatal function. Nature 263: 695–696

    Google Scholar 

  • Kilpatrick IC, Collingridge GL, Starr MS (1982) Evidence for the participation of nigrotectal γ-aminobutyrate-containing neurones in striatal and nigral-derived circling in the rat. Neuroscience 7: 207–222

    Google Scholar 

  • Kilpatrick IC, Starr MS, Fletcher A, James TA, Macleod NK (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. I. Behavioural and biochemical studies. Exp Brain Res 40: 45–54

    Google Scholar 

  • Konig JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brain stem. Williams & Wilkins Co, Baltimore

    Google Scholar 

  • Kuypers HGJM, Maisky VS (1975) Retrograde axonal transport of HRP from spinal cord to brain stem cell groups. Neurosci Lett 1: 9–14

    Google Scholar 

  • Macleod NK, James TA, Kilpatrick IC, Starr MS (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. II. Electrophysiological studies. Exp Brain Res 40: 55–61

    Google Scholar 

  • Mantyh PW (1982) The midbrain periaqueductal grey in the rat, cat and monkey: a nissl, Weil, and Golgi analysis. J Comp Neurol 204: 349–363

    Google Scholar 

  • Mantyh PW (1983) Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections. J Neurophysiol 49: 582–594

    Google Scholar 

  • Marshall JF, Ungerstedt U (1977) Striatal efferent fibers play a role in maintaining rotational behaviour in the rat. Science 198: 62–64

    Google Scholar 

  • Morrell JI, Greenberger LM, Pfaff DW (1981) Hypothalamic, other diencephalic, and telencephalic neurons that project to the dorsal midbrain. J Comp Neurol 201: 589–620

    Google Scholar 

  • Morelli M, Imperato A, Porceddu ML, Di Chiara G (1981) Role of dorsal mesencephalic reticular formation and deep layers of superior colliculus in turning behaviour elicited from the striatum. Brain Res 215: 337–341

    Google Scholar 

  • Murray EA, Coulter JD (1982) Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res 243: 201–214

    Google Scholar 

  • Oberlander C, Dumont C, Boissier JR (1977) Rotational behaviour after unilateral intranigral injection of muscimol in rats. Eur J Pharmacol 43: 389–390

    Google Scholar 

  • Olianas MC, De Montis GM, Concu A, Tagliamonte A, Di Chiara G (1978) Intranigral kainic acid: evidence for nigral nondopaminergic neurons controlling posture and behaviour in a manner opposite to the dopaminergic ones. Eur J Pharmacol 49: 223–232

    Google Scholar 

  • Olpe H-R, Schellenberg N, Koella WP (1977) Rotational behaviour induced in rats by intranigral application of GABA-related drugs and GABA antagonists. Eur J Pharmacol 45: 291–294

    Google Scholar 

  • Pellegrino LJ, Pellegrino AS, Cushman AJ (1978) A stereotaxic atlas of the rat brain. 2nd edn. Plenum Press, New York, London

    Google Scholar 

  • Pope SG, Dean P, Redgrave P (1980) Dissociation of Damphetamine-induced locomotor activity and stereotyped behaviour by lesions of the superior colliculus. Psychopharmacol 70: 297–302

    Google Scholar 

  • Pycock CJ, Marsden CD (1978) The rotating rodent: A two component system? Eur J Pharmacol 47: 167–175

    Google Scholar 

  • Reavill C, Jenner P, Leigh N, Marsden CD (1979a) Turning behaviour induced by injection of muscimol or picrotoxin into the substantia nigra demonstrates dual GABA components. Neurosci Lett 12: 323–328

    Google Scholar 

  • Reavill C, Leigh N, Jenner P, Marsden CD (1979b) Dopaminemediated circling behaviour does not involve the nigro-tectal pathway. Exp Brain Res 37: 309–316

    Google Scholar 

  • Reavill C, Leigh N, Jenner P, Marsden CD (1981) Drug-induced circling after unilateral 6-hydroxydopamine lesions of the nigro-striatal pathway is mediated via the midbrain periaqueductal grey and adjacent reticular formation (angular complex). Life Sci 29: 2357–2365

    Google Scholar 

  • Redgrave P, Dean P, Donohoe TP, Pope SG (1980) Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway. Brain Res 196: 541–546

    Google Scholar 

  • Rinvik E, Grofova I, Ottersen OP (1976) Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins. Brain Res 112: 388–394

    Google Scholar 

  • Scheel-Kruger J, Amt J, Magelund G (1977) Behavioural stimulation induced by muscimol and other GABA agonists injected into the substantia nigra. Neurosci Lett 4: 351–356

    Google Scholar 

  • Starr MS, Kilpatrick IC (1981) Distribution of γ-aminobutyrate in the rat thalamus: specific decreases in thalamic γ-aminobutyrate following lesion or electrical stimulation of substantia nigra. Neuroscience 6: 1095–1104

    Google Scholar 

  • Tarsy D, Pycock C, Meldrum B, Marsden CD (1975) Rotational behaviour induced in rats by intranigral picrotoxin. Brain Res 89: 160–165

    Google Scholar 

  • Veazey RB, Severin CM (1982) Afferent projections to the deep mesencephalic nucleus in the rat. J Comp Neurol 204: 134–150

    Google Scholar 

Download references

Author information

Affiliations

  1. University Department of Neurology, Institute of Psychiatry and The Rayne Institute, King's College Hospital Medical School, Denmark Hill, SE5 8AF, London, England

    C. Reavill, S. Muscatt, P. N. Leigh, P. Jenner & C. D. Marsden

Authors
  1. C. Reavill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Muscatt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. N. Leigh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Jenner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. D. Marsden
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Reavill, C., Muscatt, S., Leigh, P.N. et al. Enhanced GABA function in the angular complex (lateral periaqueductal grey matter and adjacent reticular formation) alters the postural component of striatal- or nigral-derived circling. Exp Brain Res 56, 1–11 (1984). https://doi.org/10.1007/BF00237436

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00237436

Key words

  • Circling behaviour
  • Angular complex
  • GABA
  • Substantia nigra
  • Striatum