Advertisement

Psychopharmacology

, Volume 75, Issue 2, pp 204–209 | Cite as

Collicular picrotoxin alleviates akinesia but not sensory neglect in rats with bilateral 6-hydroxydopamine lesions of ventral midbrain

  • Peter Redgrave
  • Paul Dean
Original Investigations

Abstract

Anatomical and biochemical investigations have suggested that GABA transmission in the superior colliculus consequent upon activity of the nigrotectal pathway is increased following 6-hydroxydopamine (6-OHDA) lesions of the ascending dopamine systems. Moreover, it has been proposed that this increase in inhibitory activity within the colliculus may be responsible for the sensory neglect commonly observed after dopamine denervation. The present experiment sought to test this proposal by examining the effects of injections of the GABA antagonist picrotoxin into the superior colliculus of 6-OHDA lesioned rats, in the hope that the neglect caused by the 6-OHDA would be reversed. However, in 33 of 36 cases studied intracollicular microinjections of picrotoxin produced no detectable improvements in orientation to sensory stimuli, although a wide range of other behavioural effects was observed. These included stereotyped exploratory movements (e.g. head waving, walking, sniffing and rearing) similar to those produced in the 6-OHDA treated rats by systemic injection of apomorphine (0.1 mg/kg). These data indicate that 6-OHDA lesions of substantia nigra and ventral midbrain areas do not produce sensory neglect simply by increasing GABA transmission within the nigrotectal pathway. Instead, such an increase in nigrotectal activity may impair production of particular kinds of movement, possibly related to exploratory behaviour.

Key words

6-Hydroxydopamine Sensorimotor deficits Superior colliculus Picrotoxin Rat 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Björklund A, Stenevi U, Dunnett SB, Iversen SD (1981) Functional reactivation of the deafferented neostriatum by nigral transplants. Nature 289:497–499Google Scholar
  2. Broadhurst PL (1960) Applications of biometrical genetics to the inheritance of behaviour. In: Eysenck HJ (ed) Experiments in personality. Routledge and Kegan Paul, London, p 3Google Scholar
  3. Brown LL, Wolfson LI (1978) Apomorphine increases glucose utilization in the substantia nigra, subthalamic nucleus and corpus striatum of rat. Brain Res 140:188–193Google Scholar
  4. Collingridge G, Kilpatrick IC, Starr MS (1980) Pharmacological manipulations of tectal GABA systems affect posture and locomotion in the rat. Brit Pharm Soc, Abstracts Dec 1980, p 124Google Scholar
  5. Dean P, Pope SG, Redgrave P, Donohoe TP (1980a) Superior colliculus lesions in rat abolish exploratory head-dipping in hole-board test. Brain Res 197:571–576Google Scholar
  6. Dean P, Redgrave P, Souki W, Lewis G (1980b) Behavioural effects of microinjections of picrotoxin into rat superior colliculus, and their modulation by intranigral 6-OHDA. Br J Pharmacol 70:145PGoogle Scholar
  7. De La Torre JC, Surgeon JW (1976) A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: The SPG method. Histochemistry 49:81–93Google Scholar
  8. Deniau UM, Hammond-Le Guyander C, Feger J (1977) Bilateral projection of nigro-collicular neurons: an electrophysiological analysis in the rat. Neurosci Lett 5:45–50Google Scholar
  9. Faull RLM, Mehler WR (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3:989–1002Google Scholar
  10. Feeney DM, Wier CS (1979) Sensory neglect after lesions of substantia nigra or lateral hypothalamus: differential severity and recovery of function. Brain Res 178:329–346Google Scholar
  11. Foreman NP, Goodale MA, Milner AD (1978) Nature of postoperative hyperactivity following lesions of the superior colliculus in the rat. Physiol Behav 21:157–160Google Scholar
  12. Grybiel AM (1978) Organisation of the nigrotectal connection: an experimental tracer study in the cat. Brain Res 143:339–348Google Scholar
  13. Herkenham M (1980) Laminar organization of thalamic projections to the rat neocortex. Science 207:532–535Google Scholar
  14. Ingle D (1973) Two visual systems in the frog. Science 181:1053–1055Google Scholar
  15. Kirvel RD, Greenfield RA, Meyer DR (1974) Multimodal sensory neglect in rats with radical unilateral posterior isocortical and superior collicular ablations. J Comp Physiol Psychol 87:156–162Google Scholar
  16. Kozlowski MR, Marshall JF (1980) Plasticity of (14C)2-deoxy-d-glucose incorporation into neostriatum and related structures in response to dopamine neuron damage and apomorphine replacement. Brain Res 197:167–183Google Scholar
  17. Marshall JF (1978) Comparison of the sensorimotor dysfunctions produced by damage to lateral hypothalamus or superior colliculus in the rat. Exp Neurol 58:203–217Google Scholar
  18. Marshall JF (1979) Sematosensory inattention after dopamine-depleting intracerebral 6-OHDA injections: spontaneous recovery and pharmacological control. Brain Res 177:311–324Google Scholar
  19. Marshall JF, Gotthelf T (1979) Sensory inattention in rats with 6-hydroxydopamine induced degeneration of ascending dopaminergic neurons: apomorphine-induced reversal of deficits. Exp Neurol 65:398–411Google Scholar
  20. Marshall JF, Richardson JS, Teitelbaum P (1974) Nigrostriatal bundle damage and the lateral hypothalamic syndrome. J Comp Physiol Psychol 87:808–830Google Scholar
  21. Marshall JF, Turner BH, Teitelbaum P (1971) Sensory neglect produced by lateral hypothalamic damage. Science 174:523–525Google Scholar
  22. Marshall JF, Ungerstedt U (1977) Apomorphine-induced restoration of drinking to thirst challenges in 6-hydroxydopamine-treated rats. Physiol Behav 17:817–822Google Scholar
  23. McCulloch J, Savaki HE, McCulloch MC, Sokoloff L (1980) Retinadependent activation by apomorphine of metabolic activity in the superficial layer of the superior colliculus. Science 207:313–315Google Scholar
  24. Mitchell I, Redgrave P (1980) Effects of partial, unilateral nigrostriatal lesions on striatal histofluorescence and behavioural indices of dopamine transmission. Br J Pharmacol 70: 47PGoogle Scholar
  25. Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A stereotaxic atlas of the rat brain Plenum Press, New YorkGoogle Scholar
  26. Pope SG, Dean P (1979) Hyperactivity, aphagia and motor disturbance following lesions of superior colliculus and underlying tegmentum in rats. Behav Neural Biol 27:433–453Google Scholar
  27. Pope SG, Dean P, Redgrave P (1980) Dissociation of d-amphetamine-induced locomotor activity and stereotyped behaviour by lesions of the superior colliculus. Psychopharmacology 70:297–302Google Scholar
  28. Redgrave P (1978) Regional changes in caudate histofluorescence following unilateral stimulation of substantia nigra in rats pretreated with α-methyl-p-tyrosine. Neurosci Lett Suppl 1:S282Google Scholar
  29. 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 196:541–546Google Scholar
  30. Redgrave P, Dean P, Souki W, Lewis G (1981) Gnawing and changes in reactivity produced by microinjections of picrotoxin into the superior colliculus of rats. Psychopharmacology 75:198–203Google Scholar
  31. Rinvik E, Grofova I, Ottersen OP (1976) Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins. Brain Res 112:388–394Google Scholar
  32. Sherman HB, Caviness VS, Ingle DJ (1979) Corticotectal connections in the gerbil. Soc Neurosci Abstr 5:120Google Scholar
  33. Somogyi P, Hodgson AJ, Smith AD (1979) An approach to tracing neuron networks in the cerebral cortex and basal ganglia. Combination of Golgi staining, retrograde transport of horseradish peroxidase and anterograde degeneration of synaptic boutons in the same material. Neuroscience 4:1805–1852Google Scholar
  34. Sprague JM, Berlucchi G, Rizzolatti G (1973) Central processing of visual information: visual centres in the brain. In: Jung R (ed) Handbook of sensory physiology, vol VII, Part 3B. Springer, Berlin Heidelberg New York, pp 271–301Google Scholar
  35. Ungerstedt U (1971) Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 367:95–122Google Scholar
  36. Wolf G (1971) Elementary histology for neuropsychologist. In: Myers RD (ed) Methods in psychobiology, vol I, Academic Press, London, pp 281–300Google Scholar
  37. Wright AK, Arbuthnott GW (1980) Non-dopamine containing efferents of substantia nigra: the pathway to the lower brain stem. J Neural Transm 47:221–226Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Peter Redgrave
    • 1
  • Paul Dean
    • 1
  1. 1.Department of PsychologyUniversity of SheffieldSheffieldEngland

Personalised recommendations