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Nitrergic Tone Influences Activity of Both Ventral Striatum Projection Neurons and Interneurons

  • Sarah Jane French
  • Henrike Hartung
Conference paper
Part of the Advances in Behavioral Biology book series (ABBI, volume 58)

Abstract

Nitric oxide (NO) is a well-established striatal neuromodulator, effecting both the activity and electrical coupling of striatal projection neurons. The NO-producing interneurons within the striatum are altered in schizophrenia brain tissue, and they may be key to the pathophysiology and future treatment of schizophrenia. We investigated in vivo the effect of locally applied NO-active drugs on the firing rate of electrophysiologically and anatomically identified, medium-sized densely spiny neurons and interneurons in the ventral striatum.

Juxtacellular recording and labelling experiments were performed on ventral striatal neurons during prefrontal cortex electrical stimulation. A NO donor, precursor or scavenger were applied microiontophoretically and single unit responses were recorded; after labelling, neurons were examined morphologically to determine neuronal type.

Correlation of electrophysiological and anatomical findings revealed four drug response profiles and four types of neurons. The nitrergic modulation of ventral striatal neurons is neuronal-type specific and may be effector-mechanism dependent, and it is involved in the gating of cortically driven ventral striatal output and the temporal and spatial synchrony of the striatal networks.

Keywords

Nitric Oxide Firing Rate Action Potential Duration Ethyl Carbamate Cholinergic Interneuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Bennett BD and Bolam JP (1993) Characterization of calretinin-immunoreactive structures in the striatum of the rat. Brain Res 609: 137–148.CrossRefPubMedGoogle Scholar
  2. Bolam JP, Wainer BH and Smith AD (1984) Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy. Neuroscience 12: 711–718.CrossRefPubMedGoogle Scholar
  3. Centonze D, Pisani A, Bonsi P, Giacomini P, Bernardi G and Calabresi P (2001) Stimulation of nitric oxide-cGMP pathway excites striatal cholinergic interneurons via protein kinase G activation. J Neurosci 21: 1393–1400.PubMedGoogle Scholar
  4. Di Giovanni G, Ferraro G, Sardo P, Galati S, Esposito E and La Grutta V (2003) Nitric oxide modulates striatal neuronal activity via soluble guanylyl cyclase: an in vivo microiontophoretic study in rats. Synapse 48: 100–107.CrossRefPubMedGoogle Scholar
  5. Fagni L and Bockaert J (1996) Effects of nitric oxide on glutamate-gated channels and other ionic channels. J Chem Neuroanat 10: 231–240.CrossRefPubMedGoogle Scholar
  6. French SJ and Totterdell S (2002) Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens. J Comp Neurol 446: 151–165.CrossRefPubMedGoogle Scholar
  7. French SJ, van Dongen YC, Groenewegen HJ and Totterdell S (2002) Synaptic convergence of hippocampal and prefrontal cortical afferents to the ventral striatum in rat. In: Nicholson LFB and Faull RL (eds) The Basal Ganglia VII. Kluwer Academic/Plenum, New York, pp 399–408.Google Scholar
  8. French SJ, Ritson GP, Hidaka S and Totterdell S (2005) Nucleus accumbens nitric oxide immunoreactive interneurons receive nitric oxide and ventral subicular afferents in rats. Neuroscience 135: 121–131.CrossRefPubMedGoogle Scholar
  9. Garthwaite J and Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57: 683–706.CrossRefPubMedGoogle Scholar
  10. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13: 4908–4923.PubMedGoogle Scholar
  11. Kawaguchi Y and Kubota Y (1996) Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16: 2701–2715.PubMedGoogle Scholar
  12. Kita H, Kosaka T and Heizmann CW (1990) Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536: 1–15.CrossRefPubMedGoogle Scholar
  13. Lauer M, Johannes S, Fritzen S, Senitz D, Riederer P and Reif A (2005) Morphological abnormalities in nitric-oxide-synthase-positive striatal interneurons of schizophrenic patients. Neuropsychobiology 52: 111–117.CrossRefPubMedGoogle Scholar
  14. Mallet N, Le Moine C, Charpier S and Gonon F (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25: 3857–3869.CrossRefPubMedGoogle Scholar
  15. O’Donnell P and Grace AA (1997) Cortical afferents modulate striatal gap junction permeability via nitric oxide. Neuroscience 76: 1–5.CrossRefPubMedGoogle Scholar
  16. Pennartz CM, Ameerun RF, Groenewegen HJ and Lopes da Silva FH (1993) Synaptic plasticity in an in vitro slice preparation of the rat nucleus accumbens. Eur J Neurosci 5: 107–117.CrossRefPubMedGoogle Scholar
  17. Pennartz CM, Groenewegen HJ and Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42: 719–761.CrossRefPubMedGoogle Scholar
  18. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 65: 113–136.CrossRefPubMedGoogle Scholar
  19. Reif A, Herterich S, Strobel A, Ehlis AC, Saur D, Jacob CP, Wienker T, Topner T, Fritzen S, Walter U, Schmitt A, Fallgatter AJ and Lesch KP (2006) A neuronal nitric oxide synthase (NOS-I) haplotype associated with schizophrenia modifies prefrontal cortex function. Mol Psychiatry 11: 286–300.CrossRefPubMedGoogle Scholar
  20. Robello M, Amico C, Bucossi G, Cupello A, Rapallino MV and Thellung S (1996) Nitric oxide and GABAA receptor function in the rat cerebral cortex and cerebellar granule cells. Neuro-science 74: 99–105.CrossRefPubMedGoogle Scholar
  21. Sardo P, Ferraro G, Di Giovanni G and La Grutta V (2003) Nitric oxide-induced inhibition on striatal cells and excitation on globus pallidus neurons: a microiontophoretic study in the rat. Neurosci Lett 343: 101–104.CrossRefPubMedGoogle Scholar
  22. Vincent SR, Johansson O, Hokfelt T, Skirboll L, Elde RP, Terenius L, Kimmel J and Goldstein M (1983) NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities. J Comp Neurol 217: 252–263.CrossRefPubMedGoogle Scholar
  23. West AR and Galloway MP (1997) Endogenous nitric oxide facilitates striatal dopamine and glutamate efflux in vivo: role of ionotropic glutamate receptor-dependent mechanisms. Neuropharmacology 36: 1571–1581.CrossRefPubMedGoogle Scholar
  24. West AR and Grace AA (2004) The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo. J Neurosci 24: 1924–1935.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of PharmacologyUniversity of OxfordOxfordUK

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