Elsevier

Neuroscience

Volume 47, Issue 3, April 1992, Pages 613-619
Neuroscience

Opposite effects of neurotensin on dopamine inhibition in different regions of the rat brain: An iontophoretic study

https://doi.org/10.1016/0306-4522(92)90170-7Get rights and content

Abstract

Anatomical, biochemical and behavioral data suggest functional interactions between dopamine and neurotensin in regions of the brain receiving a co-existent and/or distinct innervation by these two transmitters. We therefore measured and compared the effects of iontophoretically applied dopamine and neurotensin in the prefrontal and anterior cingulate cortex (coexistent innervation) vs the nucleus accumbens and neostriatum (distinct innervation) of urethane-anesthetized rats. In every region, the firing rate of most spontaneously active neurons was depressed by dopamine. Neurotensin had no effect on the same cells, except for a few nucleus accumbens units which were inhibited by the peptide. When dopamine and neurotensin were concomitantly applied, the magnitude of maximal inhibitions induced by dopamine was modified in the majority of neurons tested. A significant decrease in dopamine inhibition was observed in 100% of anterior cingulate, 74% of prefrontal cortex and 48% of accumbens units. On the contrary, in neostriatum, dopamine inhibition was significantly increased in 60% of the units tested. In every region, the remaining neurons showed less than 30% changes in dopamine responsiveness, and were therefore considered unaffected by neurotensin. In the anterior cingulate cortex, inhibitions, respectively, induced by the dopamine D1 agonist, SKF 38393, and the D2 agonist, LY 171555, were also decreased by simultaneous application of neurotensin.

Together with currently available data on the cellular localization of neurotensin receptors in rat brain, these results suggest that the modulation of dopamine inhibition by neurotensin may have opposite effects depending on whether the neurotensin receptors are located postsynaptically on target neurons (antagonistic effects) or presynaptically on dopamine terminals (potentiating effects).

References (67)

  • KalivasP.W. et al.

    Neurotensin neurons in the ventral tegmental area project to the medial nucleus accumbens

    Brain Res.

    (1984)
  • KitabgiP.

    Neurotensin modulates dopamine transmission at several levels along brain dopaminergic pathways

    Neurochem. Int.

    (1989)
  • LaitinenK. et al.

    Neurotensin and cholecystokinin microinjected into the ventral tegmental area modulate microdialysate concentrations of dopamine and metabolites in the posterior nucleus accumbens

    Brain Res.

    (1990)
  • LundbergJ.M. et al.

    Frequency and reserpine-dependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen

    Neurosci. Lett.

    (1986)
  • MarwahaJ. et al.

    Electrophysiological actions of neurotensin in rat cerebellum

    Regul. Pept.

    (1980)
  • McCarthyP.S. et al.

    The action of neurotensin on neurons in the nucleus accumbens and cerebellum of the rat

    Gen. Pharmac.

    (1979)
  • MileticV. et al.

    Neurotensin excites cat spinal neurones located in laminae I—III

    Brain Res.

    (1979)
  • MoyseE. et al.

    Distribution of neurotensin binding sites in rat brain: a light microscopic radiographic study using monoiodo-[125I]Tyr3-neurotensin

    Neuroscience

    (1987)
  • NemeroffC.B. et al.

    Neurotensin-dopamine interactions in the CNS

    Trends pharmac. Sci.

    (1985)
  • OkumaY. et al.

    Neurotensin potentiates the potassium-induced release of endogenous dopamine from rat striatal slices

    Eur. J. Pharmac.

    (1983)
  • PinnockR.D.

    Neurotensin depolarizes substantia nigra dopamine neurons

    Brain Res.

    (1985)
  • QuirionR.

    Interactions between neurotensin and dopamine in the brain: an overview

    Peptides

    (1983)
  • QuirionR. et al.

    Autoradiographic distribution of [3H]neurotensin receptors in rat brain: visualization by tritium-sensitive film

    Peptides

    (1982)
  • QuirionR. et al.

    Comparative localization of neurotensin receptors on nigrostriatal and mesolimbic dopaminergic terminals

    Brain Res.

    (1985)
  • SawadaS. et al.

    Electrical activity recorded from thin sections of the bed nucleus of the stria terminalis, and the effects of neurotensin

    Brain Res.

    (1980)
  • SeroogyK. et al.

    A subpopulation of dopaminergic neurons in rat ventral mesencephalon contains both neurotensin and cholecystokinin

    Brain Res.

    (1988)
  • SeutinV. et al.

    Electrophysiological effects of neurotensin in dopaminergic neurons of the ventral tegmental area of the rat in vitro

    Neuropharmacology

    (1989)
  • StanzioneP. et al.

    Action of neurotensin on spinal cord neurons in the rat

    Brain Res.

    (1983)
  • TanganelliS. et al.

    Neurotensin counteracts apomorphine-induced inhibition of dopamine release as studied by microdialysis in rat neostriatum

    Brain Res.

    (1989)
  • WoulfeJ. et al.

    Immunocytochemical evidence for direct connections between neurotensin-containing neurons and dopaminergic neurons in the rat ventral midbrain tegmentum

    Brain Res.

    (1989)
  • ZieglgansbergerW. et al.

    Actions of neurotensin upon single neurone activity in different regions of the rat brain

  • AndradeR. et al.

    Neurotensin selectively activates dopaminergic neurons of the substantia nigra

    Soc. Neurosci. Abstr.

    (1981)
  • AudinatE. et al.

    Neurotensin-induced excitation of neurons of the rat's frontal cortex studied intracellularly in vitro

    Expl Brain Res.

    (1989)
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