Skip to main content
SpringerLink
Log in

Locally Administered Low Nicotine-Induced Neurotransmitter Changes in Areas of Cognitive Function

  • Published:
Neurochemical Research Aims and scope Submit manuscript

The present study examined the effect of a low-dose of nicotine; below that one expects to be achieved from a single cigarette, on brain regional heterogeneity and sensitivity of catecholaminergic responses. 1 μM nicotine was infused into six brain areas via a microdialysis probe: the dorsal and ventral hippocampus, the medial temporal and prefrontal cortex, the basolateral amygdala, and the ventral tegmental area (VTA). The nicotine concentration in the brain tissue near the probe site was approximately 0.1 μM. Nicotine-induced increases and decreases could be noted in dopamine (DA), norepinephrine (NE), and serotonin (5HT) levels. In particular, DA and 5HT decreased in both hippocampal areas, while NE increased in the dorsal and decreased in the ventral hippocampus. In the cortical areas, DA and NE increased and 5HT was not significantly altered. In the amygdala all three neurotransmitters increased and in the VTA, all three decreased. Many of the nicotine-induced changes in neurotransmitter concentrations were reversed in the presence of atropine. Where nicotine induced decreases in DA and 5HT in the VTA, increases were observed in the presence of atropine. A similar reversal was seen with NE in the VTA and ventral hippocampus. In contrast, the increases in DA observed in the cortex and amygdala and the increases in NE observed in the cortex, amygdala and dorsal hippocampus were inhibited by the presence of atropine. 5HT was also significantly decreased in the amygdala and both cortical areas in the presence of atropine, where nicotine alone had no significant effect. We conclude, that at low doses, nicotine significantly alters the release of DA, NE, and 5HT – in some areas increasing, in others decreasing endogenous neurotransmitter levels. This data, in conjunction with previous experiments, indicates that the effects of nicotine are regionally heterogeneous and arise from both direct and indirect actions on various receptors and neurotransmitter systems and nicotine’s effects at low doses differ from that at higher doses. The changes in effects in the presence of atropine suggest that muscarinic acetylcholine receptors play a major role in nicotine’s actions on neurotransmitter systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S. Rossi S. Singer E. Shearman H. Sershen A. Lajtha (2005) ArticleTitleThe effects of cholinergic and dopaminergic antagonists on nicotine-induced cerebral neurotransmitter changes Neurochem. Res. 30 541–558 Occurrence Handle10.1007/s11064-005-2689-x Occurrence Handle16076024

    Article  PubMed  Google Scholar 

  2. S. Singer S. Rossi S. Verzosa A. Hashim R. Lonow T. Cooper H. Sershen A. Lajtha (2004) ArticleTitleNicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function Neurochem. Res. 29 1779–1792 Occurrence Handle10.1023/B:NERE.0000035814.45494.15 Occurrence Handle15453274

    Article  PubMed  Google Scholar 

  3. S. Rossi S. Singer E. Shearman H. Sershen A. Lajtha (2005) ArticleTitleRegional heterogeneity of nicotine effects on neurotransmitters in rat brains in vivo at low doses Neurochem. Res. 30 91–103 Occurrence Handle10.1007/s11064-004-9690-7 Occurrence Handle15756937

    Article  PubMed  Google Scholar 

  4. S. A. Tucci R. F. Genn S. E. File (2003) ArticleTitleMethyllycaconitine (MLA) blocks the nicotine evoked anxiogenic effect and 5-HT release in the dorsal hippocampus: Possible role of alpha7 receptors Neuropharmacology 44 367–373 Occurrence Handle10.1016/S0028-3908(02)00391-X Occurrence Handle12604094

    Article  PubMed  Google Scholar 

  5. P. P. Rowell (1995) ArticleTitleNanomolar concentrations of nicotine increase the release of [3H]dopamine from rat striatal synaptosomes Neurosci. Lett. 189 171–175 Occurrence Handle10.1016/0304-3940(95)11471-8 Occurrence Handle7624037

    Article  PubMed  Google Scholar 

  6. Y. Fu S. G. Matta W. Gao V. G. Brower B. M. Sharp (2000) ArticleTitleSystemic nicotine stimulates dopamine release in nucleus accumbens: Re-evaluation of the role of N-methyl-D- aspartate receptors in the ventral tegmental area J. Pharmacol. Exp. Ther. 294 458–465 Occurrence Handle10900219

    PubMed  Google Scholar 

  7. E. Toth (1996) ArticleTitleEffect of nicotine on the level of extracellular amino acids in the hippocampus of rat Neurochem. Res. 21 903–907 Occurrence Handle8895843

    PubMed  Google Scholar 

  8. M. E. Benwell D. J. Balfour (1997) ArticleTitleRegional variation in the effects of nicotine on catecholamine overflow in rat brain Eur. J. Pharmacol. 325 13–20 Occurrence Handle10.1016/S0014-2999(97)00101-5 Occurrence Handle9151933

    Article  PubMed  Google Scholar 

  9. M. Shoaib I. P. Stolerman (1995) ArticleTitleConditioned taste aversions in rats after intracerebral administration of nicotine Behav. Pharmacol. 6 375–385 Occurrence Handle11224346

    PubMed  Google Scholar 

  10. E. Toth H. Sershen A. Hashim E. S. Vizi A. Lajtha (1992) ArticleTitleEffect of nicotine on extracellular levels of neurotransmitters assessed by microdialysis in various brain regions: Role of glutamic acid Neurochem. Res. 17 265–271 Occurrence Handle10.1007/BF00966669 Occurrence Handle1352387

    Article  PubMed  Google Scholar 

  11. J. P. O’Doherty (2004) ArticleTitleReward representations and reward-related learning in the human brain: Insights from neuroimaging Curr. Opin. Neurobiol. 14 769–776 Occurrence Handle10.1016/j.conb.2004.10.016 Occurrence Handle15582382

    Article  PubMed  Google Scholar 

  12. E. D. Levin D. Sledge A. Baruah N. A. Addy (2003) ArticleTitleVentral hippocampal NMDA blockade and nicotinic effects on memory function Brain Res. Bull. 61 489–495 Occurrence Handle10.1016/S0361-9230(03)00183-7 Occurrence Handle13679247

    Article  PubMed  Google Scholar 

  13. W. H. Pan J. C. Sung S. M. Fuh (1996) ArticleTitleLocally application of amphetamine into the ventral tegmental area enhances dopamine release in the nucleus accumbens and the medial prefrontal cortex through noradrenergic neurotransmission J. Pharmacol. Exp. Ther. 278 725–731 Occurrence Handle8768724

    PubMed  Google Scholar 

  14. K. R. Ridderinkhof M. Ullsperger E. A. Crone S. Nieuwenhuis (2004) ArticleTitleThe role of the medial frontal cortex in cognitive control Science 306 443–447 Occurrence Handle10.1126/science.1100301 Occurrence Handle15486290

    Article  PubMed  Google Scholar 

  15. B. Schilstrom H. M. Svensson T. H. Svensson G. G. Nomikos (1998) ArticleTitleNicotine and food induced dopamine release in the nucleus accumbens of the rat: Putative role of alpha7 nicotinic receptors in the ventral tegmental area Neuroscience 85 1005–1009 Occurrence Handle10.1016/S0306-4522(98)00114-6 Occurrence Handle9681941

    Article  PubMed  Google Scholar 

  16. I. Sziraki H. Sershen A. Hashim A. Lajtha (2002) ArticleTitleReceptors in the ventral tegmental area mediating nicotine-induced dopamine release in the nucleus accumbens Neurochem. Res. 27 253–261 Occurrence Handle10.1023/A:1014844823534 Occurrence Handle11958525

    Article  PubMed  Google Scholar 

  17. N. Haddjeri C. Faure G. Lucas O. Mnie-Filali G. Chouvet B. Astier B. Renaud P. Blier G. Debonnel (2004) ArticleTitleIn-vivo modulation of central 5-hydroxytryptamine (5-HT1A) receptor-mediated responses by the cholinergic system Int. J. Neuropsychopharmacol. 7 391–399 Occurrence Handle10.1017/S1461145704004377 Occurrence Handle15140278

    Article  PubMed  Google Scholar 

  18. S. N. Mitchell K. M. Smith M. H. Joseph J. A. Gray (1993) ArticleTitleIncreases in tyrosine hydroxylase messenger RNA in the locus coeruleus after a single dose of nicotine are followed by time-dependent increases in enzyme activity and noradrenaline release Neuroscience 56 989–997 Occurrence Handle10.1016/0306-4522(93)90145-6 Occurrence Handle7904333

    Article  PubMed  Google Scholar 

  19. F. M. Zhou Y. Liang R. Salas L. Zhang M. Biasi ParticleDe J. A. Dani (2005) ArticleTitleCorelease of dopamine and serotonin from striatal dopamine terminals Neuron 46 65–74 Occurrence Handle10.1016/j.neuron.2005.02.010 Occurrence Handle15820694

    Article  PubMed  Google Scholar 

  20. H. Sershen A. Balla A. Lajtha E. S. Vizi (1997) ArticleTitleCharacterization of nicotinic receptors involved in the release of noradrenaline from the hippocampus Neuroscience 77 121–130 Occurrence Handle10.1016/S0306-4522(96)00425-3 Occurrence Handle9044380

    Article  PubMed  Google Scholar 

  21. Y. Gioanni C. Rougeot P. B. Clarke C. Lepouse A. M. Thierry C. Vidal (1999) ArticleTitleNicotinic receptors in the rat prefrontal cortex: Increase in glutamate release and facilitation of mediodorsal thalamo-cortical transmission Eur. J. Neurosci. 11 18–30 Occurrence Handle10.1046/j.1460-9568.1999.00403.x Occurrence Handle9987008

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Nathan Kline Institute, Orangeburg, New York, 10962, USA

    E. Shearman, S. Rossi, H. Sershen, A. Hashim & A. Lajtha

Authors
  1. E. Shearman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Sershen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Hashim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Lajtha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Sershen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shearman, E., Rossi, S., Sershen, H. et al. Locally Administered Low Nicotine-Induced Neurotransmitter Changes in Areas of Cognitive Function. Neurochem Res 30, 1055–1066 (2005). https://doi.org/10.1007/s11064-005-7132-9

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-005-7132-9

Keywords

Search

Navigation