Co-localization of GABA with other neuroactive substances in the basal ganglia

https://doi.org/10.1016/S0079-6123(06)60016-2Get rights and content

Abstract

The dorsal striatum (caudate putamen) contains two types of GABAergic medium spiny neurons (MSNs) that are distinguished by the expression of either the opioid peptide, enkephalin, or the opioid peptide, dynorphin, as well as the tachykinin substance P. Pharmacological studies suggest that these peptides modulate local neurotransmission in the striatum in response to direct and indirect dopamine agonists. In contrast, GABA appears to have minimal impact within the striatum under these conditions. The actions of the peptide cocktail are dependent on the cellular distribution of their receptors in the striatal network. The net result of their actions is a homeostatic response that regulates striatal output and balances dopamine and glutamate receptor stimulation.

Section snippets

Location of neuropeptides and receptors in MSNs

Figure 1 illustrates the circuitry and cellular location of some of the major peptides and receptors that will be discussed in this review. MSNs in both patch and matrix compartments contribute to two distinct projection pathways: striatonigral and striatopallidal (Gerfen and Young, 1988). The striatonigral pathway projects from the striatum to the internal segment of the globus pallidus (rodent entopeduncular nucleus) and the substantia nigra; these neurons are distinguished by the expression

Dopamine agonists increase neuropeptide expression in MSNs

Direct and indirect dopamine agonists induce behavioral activity in rodents that is positively correlated with neuropeptide gene expression in the striatum. Induction of striatal neuropeptides, preprodynorphin (PPD), preproenkephalin (PPE), neurotensin/neuromedin N (NT), and the SP precursor, preprotachykinin (PPT) in MSNs occurs after acute or repeated administration of the psychostimulants, cocaine, amphetamine, or methamphetamine (Castel et al., 1994; Merchant et al., 1994; Smith and

Neuropeptide regulation of local striatal circuitry

It often goes unrecognized that local regulation within the striatum has a major impact on MSN output and that endogenous inhibitory or homeostatic systems also are activated by dopamine agonists. Two of the inhibitory substrates that are critical to controlling excessive dopamine and glutamate neurotransmission in the striatum are the muscarinic cholinergic (Wang and McGinty, 1996b, Wang and McGinty, 1996d, Wang and McGinty, 1997a, Wang and McGinty, 1997b, Wang and McGinty, 1998) and

Conclusion

The studies described above suggest a model for local striatal interactions when peptides are released from MSNs (Fig. 5). When dopamine stimulates D1 receptors on striatonigral MSNs, for example, SP and dynorphin are released from local collaterals. SP stimulates NK-1 receptors, predominantly expressed by cholinergic interneurons, and stimulates ACh release. Dynorphin stimulates KORs that presynaptically inhibit dopamine and glutamate release. The net effect is a local regulation of striatal

Acknowledgment

The studies from the author's laboratory were supported by NIH DA03982.

References (88)

  • G.R. Hanson et al.

    Characterization of methamphetamine effects on the striatal-nigral dynorphin system

    Eur. J. Pharmacol.

    (1988)
  • G.R. Hanson et al.

    Response by the neurotensin systems of the basal ganglia to cocaine treatment

    Eur. J. Pharmacol.

    (1989)
  • C. Heidbreder et al.

    The kappa-opioid receptor agonist U-69593 attenuates cocaine-induced behavioral sensitization in the rat

    Brain Res.

    (1993)
  • C. Heidbreder et al.

    Differential role of delta receptors in the development and expression of behavioral sensitization to cocaine

    Eur. J. Pharmacol.

    (1996)
  • M.H. Heijna et al.

    Opioid receptor-mediated inhibition of dopamine and acetylcholine release from slices of rat nucleus accumbens, olfactory tubercle and frontal cortex

    Eur. J. Pharmacol.

    (1990)
  • D.N.C. Jones et al.

    Delta-opioid receptor antagonists attenuate motor activity induced by amphetamine but not cocaine

    Eur. J. Pharmacol.

    (1993)
  • E.A. Jones et al.

    The role of striatal GABAA receptors in dopamine agonist-induced behavior and gene expression

    Brain Res.

    (1999)
  • E.A. Jones et al.

    Intrastriatal GABAA receptor blockade does not alter D1/D2 interactions in the intact rat striatum

    Neuroscience

    (2001)
  • T. Kaneko et al.

    Substance P receptor-immunoreactive neurons in the rat striatum are segregated into somatostatinergic and cholinergic aspiny neurons

    Brain Res.

    (1993)
  • C.J. Lacey et al.

    GABAB receptors at glutamatergic synapses in the rat striatum

    Neuroscience

    (2005)
  • C. Le Moine et al.

    Delta opioid receptor gene expression in the mouse forebrain: localization in cholinergic neurons of the striatum

    Neuroscience

    (1994)
  • I.M. Maisonneuve et al.

    U50,488, a kappa opioid receptor agonist, attenuates cocaine-induced increases in dialysate dopamine in the nucleus accumbens of rats

    Neurosci. Lett.

    (1994)
  • C.K. Meshul et al.

    Kappa opioid receptor immunoreactivity in nucleus accumbens shell and caudate-putamen is primarily associated with synaptic vesicles in axons

    Neuroscience

    (2000)
  • M.E. Meyer et al.

    Behavioral effects of the mu-opioid peptide agonists DAMGO, DALDA, and PL017 on locomotor activities

    Pharmacol. Biochem. Behav.

    (1993)
  • A. Parent et al.

    Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop

    Brain Res. Rev.

    (1995)
  • F. Petit et al.

    Further evidence for a role of delta opiate receptor in the presynaptic regulation of newly synthesized dopamine release

    Eur. J. Pharmacol.

    (1986)
  • S.M. Rawls et al.

    Delta opioid receptors regulate calcium-dependent, amphetamine-evoked glutamate levels in the striatum: an in vivo microdialysis study

    Brain Res.

    (2000)
  • N.T. Sandor et al.

    Effect of opiate antagonists on striatal acetylcholine and dopamine release

    Brain Res. Bull.

    (1992)
  • A.J. Saylor et al.

    BDNF heterozygous mice demonstrate age-related changes in striatal and nigral gene expression

    Exp. Neurol.

    (2006)
  • T.S. Shippenberg et al.

    The delta-opioid receptor antagonist naltrindole prevents sensitization to the conditioned rewarding effects of cocaine

    Eur. J. Pharmacol.

    (1995)
  • T.S. Shippenberg et al.

    Motivational properties of opioids: evidence that an activation of delta-receptors mediates reinforcement processes

    Brain Res.

    (1987)
  • N.A. Singh et al.

    N-Methyl-D-aspartate receptors mediate dopamine-induced changes in extrapyramidal and limbic dynorphin systems

    Brain Res.

    (1991)
  • A.J.W. Smith et al.

    Acute amphetamine and methamphetamine alter opioid peptide mRNA expression in the rat striatum

    Mol. Brain Res.

    (1994)
  • H. Steiner et al.

    Enkephalin regulates acute D2 receptor antagonist-induced immediate-early gene expression in striatal neurons

    Neurosci.

    (1999)
  • J.A. Tzaferis et al.

    Kappa opioid receptor stimulation decreases amphetamine-induced behavior and neuropeptide mRNA expression in the striatum

    Mol. Brain Res.

    (2001)
  • M. Ukai et al.

    Systemic administration of dynorphin A (1–13) markedly inhibits different behavioural responses induced by cocaine in the mouse

    Neuropharmacol.

    (1992)
  • J.Q. Wang et al.

    Scopolamine augments c-fos and zif/268 mRNA expression induced by the full D1 dopamine receptor agonist SKF-82958 in the intact rat striatum

    Neuroscience

    (1996)
  • J.Q. Wang et al.

    Intrastriatal injection of the metabotropic glutamate receptor antagonist MCPG attenuates acute amphetamine-stimulated neuropeptide mRNA expression in rat striatum

    Neurosci. Lett.

    (1996)
  • J.Q. Wang et al.

    Muscarinic receptors regulate striatal neuropeptide gene expression in normal and amphetamine-treated rats

    Neuroscience

    (1996)
  • J.Q. Wang et al.

    Intrastriatal injection of a muscarinic receptor agonist and antagonist regulates striatal neuropeptide mRNA expression in normal and amphetamine-treated rats

    Brain Res.

    (1997)
  • Z.-B. You et al.

    The striatonigral dynorphin pathway of the rat studied with in vivo microdialysis--II. Effects of dopamine D1 and D2 receptor agonists

    Neuroscience

    (1994)
  • W. Zhou et al.

    GABAB receptor stimulation decreases amphetamine-induced neuropeptide mRNA expression in the striatum of rats

    Brain Res.

    (2004)
  • A.K. Afifi

    The basal ganglia: functional anatomy and physiology, Part 1

    J. Child Neurol.

    (1994)
  • J.J. Anderson et al.

    Dopamine D1 receptor-stimulated release of acetylcholine in rat striatum is mediated by activavtion of striatal neurokinin1 receptors

    J. Pharmacol. Exper. Therap.

    (1994)
  • Cited by (34)

    • New insights into pathogenesis of L-DOPA-induced dyskinesia

      2021, NeuroToxicology
      Citation Excerpt :

      The enkephalins derived from the precursor preproenkephalin A were highly expressed in the indirect pathway, while the opioid peptides derived from preproenkephalin B were abundantly expressed in the direct pathway (Cuello and Paxinos, 1978; Gerfen et al., 1990). This suggested that the opioid system could participate in the development of PD and LID through the regulation of direct and indirect pathways (Aubert et al., 2007; Calon et al., 2002a, 2002b; McGinty, 2007). Additionally, long-term l-DOPA treatment reduced the level of OPRM1 binding in caudate and putamen, while the level of OPRM1 in premotor and motor cortex was increased (Johansson et al., 2001), the regional difference is worthy of attention and warrants further investigation to explain the connotation behind this change.

    • Methylphenidate and μ opioid receptor interactions: A pharmacological target for prevention of stimulant abuse

      2011, Neuropharmacology
      Citation Excerpt :

      Another issue raised by our findings is the potential interaction between MOPR and dopamine receptors in the mediation of MPH-induced place preference. MOPR co-localizes with the D1-receptor, substance P and dynorphin in the striatal GABAergic medium spiny neurons (Georges et al., 1999; Guttenberg et al., 1996; McGinty, 2007), which contribute to the striatonigral (direct) pathway. MOPR co-localizes with the D2-receptor mainly in the striatal enkephalinergic GABA neurons (Ambrose et al., 2004; McGinty, 2007), which play an important role in the striatopallidal (indirect) pathway.

    • Substance P selectively modulates GABA<inf>A</inf> receptor-mediated synaptic transmission in striatal cholinergic interneurons

      2010, Neuropharmacology
      Citation Excerpt :

      The modulation of striatal microcircuitry can have a great influence on striatal output (for review, see Tepper et al., 2004; Wilson, 2007). The tachykinin family of neuropeptides including substance P (SP) is expressed in approximately 50% of MSNs and co-localized with GABA in the axonal terminals of MSNs (Bolam et al., 1983; Tepper et al., 2004; Tepper and Bolam, 2004; McGinty, 2007). Three subtypes of neurokinin (NK) receptors have been identified in the brain: NK1, NK2, and NK3 (Helke et al., 1990; Nakanishi, 1991; Otsuka and Yoshioka, 1993).

    View all citing articles on Scopus
    View full text