Skip to main content

Anatomical Characteristics of Norepinephrine Axons in the Prefrontal Cortex: Unexpected Findings That May Indicate Low Activity State in Naïve Animals

  • Chapter
Monoaminergic Modulation of Cortical Excitability

The catecholamine norepinephrine (NE) critically regulates information processing within the central nervous system. Along with dopamine (DA) and serotonin (5-HT; 5-hydroxytryptamine), the NE system forms an essential component of the modulatory brainstem innervation that ascends directly to the cerebral cortex without first being relayed through the thalamus. Within the prefrontal cortex (PFC) in particular, NE is known to modulate the essential cognitive and affective functions of this region, with animal studies demonstrating that normal NE innervation to the PFC is necessary for working memory, attention, and arousal (Robbins, 1984; Aston-Jones et al., 1999; Berridge, 2001; Berridge and Waterhouse, 2003; Arnsten and Li, 2005; Lapiz and Morilak, 2006).

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abercrombie, E.D. and Jacobs, B.L. (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely-moving cats. I. Acutely presented stressful and nonstressful stimuli. J. Neurosci. 7, 2837-2843.

    CAS  PubMed  Google Scholar 

  • Abercrombie, E.D., Keller, R.W. and Zigmond, M.J. (1988) Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 27, 897-904.

    CAS  PubMed  Google Scholar 

  • Abercrombie, E.D., Keefe, K.A., DiFrischia, D.S. and Zigmond, M.J. (1989) Differential effects of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J. Neurochem. 52, 1655-1658.

    CAS  PubMed  Google Scholar 

  • Adell, A., Garcia-Marquez, C., Armario, A. and Gelpi, E. (1988) Chronic stress increases serotonin and noradrenaline in the rat brain and sensitizes their responses to further acute stress. J. Neurochem. 50, 1678-1681.

    CAS  PubMed  Google Scholar 

  • Adell, A., Garcia-Marquez, C., Armario, A. and Gelpi, E. (1989) Chronic administration of clomipramine prevents the increase in serotonin and noradrenalin induced by chronic stress. Psychopharmacology 99, 22-26.

    CAS  PubMed  Google Scholar 

  • Ader, J.-P., Room, P., Postema, F. and Korf, J. (1980) Bilateral diverging axon collaterals and contralateral projections from rat locus coeruleus neurons. J. Neural Transm. 49, 207-218.

    CAS  PubMed  Google Scholar 

  • Angulo, J.A., Printz, D., Ledoux, M. and McEwen, B.S. (1991) Isolation stress increases tyrosine hydroxylase mRNA in the locus coeruleus and midbrain and decreases proen-kephalin mRNA in the striatum and nucleus accumbens. Molec. Brain Res. 11, 301-308.

    CAS  PubMed  Google Scholar 

  • Anisman, H. and Zacharko, R.M. (1990) Multiple neurochemical and behavioral conse-quences of stressors: implications for depression. Pharmacol Therapeutics 46, 119-136.

    CAS  Google Scholar 

  • Aoki, C. (1992) Beta-adrenergic receptors: astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry. J. Neurosci. 12, 781-792.

    CAS  PubMed  Google Scholar 

  • Aoki, C., Go, C.-G., Venkatesan, C. and Kurose, H. (1994) Perikaryal and synaptic localiza-tion of alpha2A-adrenergic receptor-like immunoreactivity. Brain Res. 650, 181-204.

    CAS  PubMed  Google Scholar 

  • Aoki, C., Venkatesan, C., Go, C.-G., Forman, R. and Kurose, H. (1998) Cellular and subcellu-lar sites for noradrenergic action in the monkey dorsolateral prefrontal cortex as revealed by the immunocytochemical localization of noradrenergic receptors and axons. Cereb. Cortex 8, 269-277.

    CAS  PubMed  Google Scholar 

  • Apparsundaram, S., Schroeter, S., Giovanetti, E. and Blakely, R.D. (1998a) Acute regulation of norepinephrine transport. II. PKC-modulated surface expression of human norepineph-rine transporter proteins. J. Pharm. Exp. Ther. 287, 744-751.

    CAS  Google Scholar 

  • Apparsundaram, S., Galli, A., DeFelice, L.J., Hartzell, H.C. and Blakely, R.D. (1998b) Acute regulation of norepinephrine transport. I. Protein kinase C-linked muscarinic receptors influence transport capacity and transporter density in SK-N-SH cells. J. Pharm. Exp. Ther. 287, 733-743.

    CAS  Google Scholar 

  • Armstrong-James, M. and Fox, K. (1983) Effects of iontophoresed noradrenaline on the spon-taneous activity of neurons in rat primary somatosensory cortex. J. Physiol. 355, 427-447.

    Google Scholar 

  • Arnsten, A. and Goldman-Rakic, P. (1985) a2-Adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged non-human primates. Science 230, 1273-1276.

    CAS  PubMed  Google Scholar 

  • Arnsten, A., Steere, J. and Hunt, R. (1996) The contribution of alpha2-noradrenergic mecha-nisms to prefrontal cortical cognitive function. Arch. Gen. Psychiatry 53, 448-455.

    CAS  PubMed  Google Scholar 

  • Arnsten, A.F. (2000) Stress impairs prefrontal cortical function in rats and monkeys: Role of dopamine D1 and norepinephrine a-1 receptor mechanisms. Prog. Brain Res. 126, 183-192.

    CAS  PubMed  Google Scholar 

  • Arnsten, A.F. and Li, B.M. (2005) Neurobiology of executive functions: Catecholamine influ-ences on prefrontal cortical functions. Biol. Psychiatry 57, 1377-1384.

    CAS  PubMed  Google Scholar 

  • Arnsten, A.F., Steere, J.C., Jentsch, D.J. and Li, B.M. (1998) Noradrenergic influences on prefrontal cortical cognitive function: opposing actions at postjunctional alpha-1 versus alpha-2-adrenergic receptors. Adv. Pharmacol. 42, 764-767.

    CAS  PubMed  Google Scholar 

  • Asan, E. (1993) Comparative single and double immunolabelling with antisera against cate-cholamine biosynthetic enzymes: criteria for the identification of dopaminergic, noradren-ergic and adrenergic structures in selected rat brain areas. Histochemistry 99, 427-442.

    CAS  PubMed  Google Scholar 

  • Aston-Jones, G., Fajkowski, J. and Cohen, J. (1999) Role of the locus coeruleus in attention and behavioral flexibility. Biol. Psychiatry 46, 1309-1320.

    CAS  PubMed  Google Scholar 

  • Aston-Jones, G., Zhu, Y. and Card, J.P. (2004) Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: possible interneuronal pool. J. Neurosci. 24, 2313-2321.

    CAS  PubMed  Google Scholar 

  • Aston-Jones, G., Valentino, R.J., VanBockstaele, E.J. and Meyerson, A.T. (1994) Locus coeruleus, stress, and PTSD: neurobiological and clinical parallels. In: M.M. Murbur (ed.), Catecholamine Function in PTSD: Emerging Concepts. American Psychiatric Press, Washington, DC, pp. 17-62.

    Google Scholar 

  • Audet, M.A., Doucet, G., Oleskevich, S. and Descarries, L. (1988) Quantified regional and laminar distribution of the noradrenaline innervation in the anterior half of the adult rat cerebral cortex. J. Comp. Neurol. 274, 307-318.

    CAS  PubMed  Google Scholar 

  • Avery, R.A., Franowicz, J.S., Studholme, C., van Dyck, C.H. and Arnsten, A.F. (2000) The alpha-2A-adrenoceptor agonist, guanfacine, increases regional cerebral blood flow in dor-solateral prefrontal cortex of monkeys performing a spatial working memory task. Neuro-psychopharmacology 23, 240-249.

    CAS  Google Scholar 

  • Bauer, M.E. and Tejani-Butt, S.M. (1992) Effects of repeated administration of desipramine or electroconvulsive shock on norepinephrine uptake sites measured by [3H] nisoxetine autoradiography. Brain Res. 582, 208-214.

    CAS  PubMed  Google Scholar 

  • Beaudet, A. and Descarries, L. (1978) The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 3, 851-860.

    CAS  PubMed  Google Scholar 

  • Beaudet, A. and Descarries, L. (1984) Fine structure of monoamine axon terminals in cerebral cortex. In: L. Descarries, T.R. Reader and H.H. Jasper (eds.), Monoamine Innervation of the Cerebral Cortex. Liss, New York, pp. 77-93.

    Google Scholar 

  • Benmansour, S., Altamirano, A.V., Jones, D.J., Sanchez, T.A., Gould, G.G., Pardon, M.-C., Morilak, D.A. and Frazer, A. (2004) Regulation of the norepinephrine transporter by chronic administration of antidepressants. Biol. Psychiatry 55, 313-316.

    CAS  PubMed  Google Scholar 

  • Berridge, C.W. (2001) Arousal and attention-related actions of the locus coeruleus-noradrenergic system: potential target in the therapeutic actions of amphetamine-like stimulants. In: M.V. Solanto, A.F.T. Arnsten and F.X. Castellanos (eds.), Stimulant Drugs and ADHD. Oxford University, New York, pp. 158-184.

    Google Scholar 

  • Berridge, C.W. and Waterhouse, B.D. (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42, 33-84.

    Google Scholar 

  • Biederman, J. and Spencer, T. (1999) Attention-deficit/hyperactivity disorder (ADHD) as a noradrenergic disorder. Biol. Psychiatry 46, 1234-1242.

    CAS  PubMed  Google Scholar 

  • Birnbaum, S.G., Gobeske, K.T., Auerbach, J., Taylor, J.R. and Arnsten, A.F. (1999) A role for norepinephrine in stress-induced cognitive deficits: a-1-adrenoceptor mediation in the pre-frontal cortex. Biol. Psychiatry 46, 1266-1274.

    CAS  PubMed  Google Scholar 

  • Blakely, R.D. and Bauman, A.L. (2000) Biogenic amine transporters: regulation in flux. Curr. Opin. Neurobiol. 10, 328-336.

    CAS  PubMed  Google Scholar 

  • Bremner, J.D., Krystal, K.H., Soutwick, S.M. and Charney, D.S. (1996) Noradrenergic mechanisms in stress and anxiety. II. Clinical studies. Synapse 23, 39-51.

    CAS  PubMed  Google Scholar 

  • Brown, E.R., Coker, G.T. and O’Malley, K.L. (1987) Organization and evolution of the rat tyrosine hydroxylase gene. Biochemistry 26, 5208-5212.

    CAS  PubMed  Google Scholar 

  • Bunney, B.S. and Aghajanian, G.K. (1976) Dopamine and norepinephrine innervated cells in the rat prefrontal cortex: pharmacological differentiation using microiontophoretic tech-niques. Life Sci. 19, 1783-1792.

    CAS  PubMed  Google Scholar 

  • Bymaster, F.P., Katner, J.S., Nelson, D.L., Hemrick-Luecke, S.K., Threlkeld, P.G., Heiligenstein, J.H., Morin, S.M., Gehlert, D.R. and Perry, K.W. (2002) Atomoxetine increases extracellular levels of norepinephrine and dopamine in the prefrontal cortex of the rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27, 699-711.

    CAS  PubMed  Google Scholar 

  • Callado, L.F., Meana, J.J. and Grijalba, B. (1998) Selective increase of alpha2-adrenoceptor agonist binding sites in brains of depressed suicide victims. J. Neurochem. 70, 1114-1123.

    CAS  PubMed  Google Scholar 

  • Campbell, D.G., Hardie, D.G. and Vulliet, P.R. (1986) Identification of the four phosphoryla-tion sites in the N-terminal region of tyrosine hydroxylase. J. Biol. Chem. 261, 10489-10492.

    CAS  PubMed  Google Scholar 

  • Cass, W.A. and Gerhardt, G.A. (1995) In vivo assessment of dopamine uptake in rat medial prefrontal cortex: comparison with dorsal striatum and nucleus accumbens. J. Neurochem. 65, 201-207.

    CAS  PubMed  Google Scholar 

  • Charney, D.S., Bremner, J.D. and Redmond, D.E. (1995) Noradrenergic substrates for anxiety and fear. In: F.E. Bloom and D.J. Kupfer (eds.), Psychopharmacology: The Fourth Gen-eration of Progress. Raven Press, New York, pp. 387-395.

    Google Scholar 

  • Christenson, J.G., Dairman, W. and Udenfriend, S. (1972) On the identity of DOPA decar-boxylase and 5-hydroxytryptophan decarboxylase. Proc. Natl. Acad. Sci. 69, 343-347.

    CAS  PubMed  Google Scholar 

  • Ciliax, B., Heilman, C., Demchyshyn, L., Pristupa, Z., Ince, E., Hersch, S., Niznik, H. and Levey, A. (1995) The dopamine transporter: immunocytochemical characterization and localization in brain. J. Neurosci. 15, 1714-1723.

    CAS  PubMed  Google Scholar 

  • Conti, L.H. and Foote, S.L. (1996) Reciprocal cross-desensitization of locus coeruleus elec-trophysiological responsivity to corticotrophin-releasing factor and stress. Brain Res. 722, 19-29.

    CAS  PubMed  Google Scholar 

  • Cooper, J.R., Bloom, F.E. and Roth, R.H. (1991) The Biochemical Basis of Neuropharmacol-ogy, 6th Edition. New York: Oxford University Press.

    Google Scholar 

  • Cordero, M.I., Kruyt, N.D. and Sandi, C. (2003) Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to nov-elty. Brain Res. 970, 242-245.

    CAS  PubMed  Google Scholar 

  • Curtis, A.L., Pavcovich, L.A., Grigoriadis, D.E. and Valentino, R.J. (1995) Previous stress alters corticotropin-releasing factor neurotransmission in the locus coeruleus. Neurosci-ence 65, 541-550.

    CAS  Google Scholar 

  • Descarries, L. and Mechawar, N. (2000) Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Prog. Brain Res. 125, 27-47.

    CAS  PubMed  Google Scholar 

  • Descarries, L., Watkins, K. and Lapierre, Y. (1977) Noradrenergic axon terminals in the cere-bral cortex of rat. III. Topometric ultrastructural analysis. Brain Res. 133, 197-222.

    CAS  PubMed  Google Scholar 

  • Descarries, L., Reader, T.A. and Jasper, H.H., eds (1984) Monoamine Innervation of Cerebral Cortex. Alan R. Liss, New York.

    Google Scholar 

  • Drevets, W.C., Videen, T.O., Price, J.L., Preskorn, S.H., Carmichael, S.T. and Raichle, M.E. (1992) A functional anatomical study of unipolar depression. J. Neurosci. 12, 3628-3641.

    CAS  PubMed  Google Scholar 

  • Emson, P.C. and Koob, G.F. (1978) The origin and distribution of dopamine-containing affer-ents to the rat prefrontal cortex. Brain Res. 142, 249-267.

    CAS  PubMed  Google Scholar 

  • Ernst, M., Liebenauer, L., King, A., Fitzgerald, G.A., Cohen, R.A. and Zametkin, A.J. (1994) Reduced brain metabolism in hyperactive girls. J. Am. Acad. Child Adolesc. Psychiatry 33, 858-868.

    CAS  PubMed  Google Scholar 

  • Fallon, J.H. and Loughlin, S.E. (1982) Monoamine innervation of the forebrain: collateraliza-tion. Brain Res. Bull. 9, 295-307.

    CAS  Google Scholar 

  • Fallon, J.H. and Loughlin, S.E. (1987) Monoamine innervation of cerebral cortex and a theory of the role of monoamines in cerebral cortex and basal ganglia. In: E.G. Jones and A. Peters (eds.), Cerebral Cortex. Plenum, New York, pp. 41-127.

    Google Scholar 

  • Feenstra, M.G.P., Botterblom, M.H.A. and Matenbroek, S. (2000) Dopamine and noradrena-line efflux in the prefrontal cortex in light and dark period: effects of novelty and handling and comparisons to the nucleus accumbens. Neuroscience 100, 741-748.

    CAS  PubMed  Google Scholar 

  • Finlay, J.M., Zigmond, M.J. and Abercrombie, E.D. (1995) Increased dopamine and norepi-nephrine release in medial prefrontal cortex induced by acute and chronic stress: effects of diazepam. Neuroscience 64, 619-628.

    CAS  PubMed  Google Scholar 

  • Finlay, J.M., Jedema, H.P., Rabinovic, A.D., Mana, M.J., Zigmond, M.J. and Sved, A.F. (1997) Impact of corticotropin-releasing hormone on extracellular norepinephrine in pre-frontal cortex after chronic cold stress. J. Neurochem. 69, 144-150.

    Article  CAS  PubMed  Google Scholar 

  • Foote, S.L. (1985) Anatomy and physiology of brain monoamine systems. Psychiatry 3, 1-14.

    Google Scholar 

  • Foote, S.L., Bloom, F.E. and Oliver, A.P. (1975) Effects of putative neurotransmitters on neuronal activity in monkey auditory cortex. Brain Res. 86, 229-242.

    CAS  PubMed  Google Scholar 

  • Foote, S.L., Bloom, F.E. and Aston-Jones, G. (1983) Nucleus locus coeruleus: new evidence of anatomical and physiological specificity. Physiol. Rev. 63, 844-914.

    CAS  PubMed  Google Scholar 

  • Frazer, A. (2000) Norepinephrine involvement in antidepressant action. J. Clin. Psychiat. 61 (Suppl 10), 25-30.

    CAS  Google Scholar 

  • Frazer, A. and Benmansour, S. (2002) Delayed pharmacological effects of antidepressants. Mol. Psychiatry 7, S23-S28.

    CAS  PubMed  Google Scholar 

  • Gambarana, C., Scheggi, S., Tagliamonte, A., Tolu, P. and DeMontis, M.G. (2001) Animal models for the study of antidepressant activity. Br. Res. Protocols 7, 11-20.

    CAS  Google Scholar 

  • Garris, P.A. and Wightman, R.M. (1994) Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltametric study. J. Neurosci. 14, 442-450.

    CAS  PubMed  Google Scholar 

  • Garris, P.A., Collins, L.B., Jones, S.R. and Wightman, R.M. (1993) Evoked extracellular dopamine in vivo in the medial prefrontal cortex. J. Neurochem. 61, 637-647.

    Article  CAS  PubMed  Google Scholar 

  • Gaspar, P., Berger, B., Febvret, A., Vigny, A. and Henry, J.P. (1989) Catecholamine innerva-tion of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-beta-hydroxylase. J. Comp. Neurol. 279, 249-271.

    CAS  PubMed  Google Scholar 

  • Goldman-Rakic, P.S., Lidow, M.S. and Gallager, D.W. (1990) Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complimentarity of their subtypes in the pri-mate prefrontal cortex. J. Neurosci. 10, 2125-2138.

    CAS  PubMed  Google Scholar 

  • Grant, M.M. and Weiss, J.M. (2001) Effects of chronic antidepressant drug administration and electroconvulsive shock on locus coeruleus electrophysiological activity. Biol. Psychiatry 49, 117-129.

    CAS  PubMed  Google Scholar 

  • Gresch, P.J., Sved, A.F., Zigmond, M.J. and Finlay, J.M. (1994) Stress-induced sensitization of dopamine and norepinephrine efflux in medial prefrontal cortex of the rat. J. Neuro-chem. 63, 575-583.

    CAS  Google Scholar 

  • Gresch, P.J., Sved, A.F., Zigmond, M.J. and Finlay, J.M. (1995) Local influences of endoge-nous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J. Neuro-chem. 65, 111-116.

    CAS  Google Scholar 

  • Grzanna, R. and Fritschy, J.-M. (1991) Efferent projections of different subpopulations of central noradrenergic neurons. In: C.D. Barnes and O. Pompeiano (eds.), Progress in Brain Research. Elsevier, New York, pp. 89-101.

    Google Scholar 

  • Gu, H.H., Wall, S. and Rudnick, G. (1996) Ion coupling stoichiometry for the norepinephrine transporter in membrane vesicles from stably transfected cells. J. Biol. Chem. 271, 6911-6919.

    CAS  PubMed  Google Scholar 

  • Guitart, X., Kogan, J.H., Berhow, M., Terwilliger, R.Z., Aghajanian, G.K. and Nestler, E.J. (1993) Lewis and Fischer rat strains display differences in biochemical, electrophysiological and behavioral parameters: studies in the nucleus accumbens and locus coeruleus of drug naive and morphine-treated animals. Brain Res. 611, 7-17.

    CAS  PubMed  Google Scholar 

  • Haycock, J.W. (1990) Involvement of serine-31 in phosphorylation of tyrosine hydroxylase in PC12 cells. J. Biol. Chem. 265, 11682-11691.

    CAS  PubMed  Google Scholar 

  • Hebert, C., Habimana, A., Elie, R. and Reader, T.A. (2001) Effects of chronic antidepressant treatments on 5-HT and NA transporters in rat brain: an autoradiographic study. Neuro-chem. Int. 38, 63-74.

    CAS  Google Scholar 

  • Henry, J.P., Sagne, C., Bedet, C. and Gasnier, B. (1998) The vesicular monoamine transporter: from chromaffin granule to brain. Neurochem. Int. 32, 227-246.

    CAS  PubMed  Google Scholar 

  • Hersch, S.M., Yi, H., Heilman, C.J., Edwards, R.H. and Levey, A.I. (1997) Subcellular local-ization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J. Comp. Neurol. 388, 211-227.

    CAS  PubMed  Google Scholar 

  • Hoffman, B.J., Hansson, S.R., Mezey, E. and Palkovits, M. (1998) Localization and dynamic regulation of biogenic amine transporters in the mammalian central nervous system. Front. Neuroendocrinol. 19, 187-231.

    CAS  PubMed  Google Scholar 

  • Hökfelt, T., Johansson, O., Fuxe, K., Goldstein, M. and Park, D. (1977) Immunohistochemical studies on the localization and distribution of monoamine neuron systems in the rat brain. II. Tyrosine hydroxylase in the telencephalon. Med. Biol. 55, 21-40.

    PubMed  Google Scholar 

  • Horn, A.S. (1973) Structure-activity relations for the inhibition of catecholamine uptake into synaptosomes from noradrenaline and dopaminergic neurons in rat brain homogenates. Br. J. Pharmacol. 47, 332-338.

    CAS  PubMed  Google Scholar 

  • Huang, Y.H., Maas, J.W. and Hu, G.H. (1980) The time course of noradrenergic pre- and postsynaptic activity during chronic desipramine treatment. Eur. J. Pharmacol. 68, 41-47.

    CAS  PubMed  Google Scholar 

  • Ichikawa, S., Sasaoka, T. and Nagatsu, T. (1991) Primary structure of mouse tyrosine hydroxylase deduced from its cDNA. Biochem. Biophys. Res. Commun. 176, 1610-1616.

    CAS  PubMed  Google Scholar 

  • Invernizzi, R.W., Parini, S., Sacchetti, G., Fracasso, C., Caccia, S., Annoni, K. and Samanin, R. (2001) Chronic treatment with reboxetine by osmotic pumps facilitates its effect on extracellular noradrenaline and may desensitize alpha2-adrenoceptors in the prefrontal cortex. Br. J. Pharmacol. 132, 183-188.

    CAS  PubMed  Google Scholar 

  • Jayanthi, L.D., Samuvel, D.J. and Ramamoorthy, S. (2004) Regulated internalization and phosphorylation of the native norepinephrine transporter in response to phorbol esters: evidence for localization in lipid rafts and lipid raft-mediated internalization. J. Biol. Chem. 279, 19315-19326.

    CAS  PubMed  Google Scholar 

  • Jedema, H., Sved, A., Zigmond, M. and Finlay, J. (1999) Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols. Brain Res. 830, 211-217.

    CAS  PubMed  Google Scholar 

  • Jedema, H.P. and Grace, A.A. (2003) Chronic exposure to cold stress alters electrophysiologi-cal properties of locus coeruleus neurons recorded in vitro. Neuropsychopharmacology 28, 63-72.

    PubMed  Google Scholar 

  • Jedema, H.P., Finlay, J.M., Sved, A.F. and Grace, A.A. (2001) Chronic cold exposure potenti-ates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol. Psychiatry 49, 351-359.

    CAS  PubMed  Google Scholar 

  • Johnson, E.S., Roberts, M.H.T. and Straughan, D.W. (1969) The responses of cortical neu-rones to monoamines under differing anaesthetic conditions. J. Physiol. 203, 261-280.

    CAS  PubMed  Google Scholar 

  • Jones, B.E. and Yang, T.Z. (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. Comp. Neurol. 242, 56-92.

    CAS  PubMed  Google Scholar 

  • Jordan, S., Kramer, G.L., Zukar, P.K., Moeller, M. and Petty, F. (1994) In vivo biogenic amine efflux in medial prefrontal cortex with imipramine, fluoxetine, and fluvoxamine. Synapse 18, 294-297.

    CAS  PubMed  Google Scholar 

  • Kasamatu, T. and Heggelund, P. (1982) Single cell responses in cat visual cortex to visual stimulation during iontophoresis of noradrenaline. Exp. Brain Res. 45, 317-327.

    Google Scholar 

  • Kendler, K.S., Kessler, R.C., Walters, E.E., MacLean, C., Neale, M.C., Heath, A.C. and Eaves, L.J. (1995) Stressful life events, genetic liability, and onset of an episode of major depression in women. Am. J. Psychiatry 152, 833-842.

    CAS  PubMed  Google Scholar 

  • Kent, J.M. (2000) SNaRIs, NaSSAs, and NaRIs: new agents for the treatment of depression. Lancet 355, 911-918.

    CAS  PubMed  Google Scholar 

  • Klimek, V., Stockmeier, C., Overholser, J., Meltzer, H.Y., Kalka, S., Dilley, G. and Ordway, G.A. (1997) Reduced levels of norepinephrine transporters in the locus coeruleus in major depression. J. Neurosci. 17, 8451-8458.

    CAS  PubMed  Google Scholar 

  • Komori, K., Kunimi, Y., Yamaoka, K., Ito, T., Kasahara, Y. and Nagatsu, I. (1992) Semiquan-titative analysis of immunoreactivities of tyrosine hydroxylase and aromatic L-amino acid decarboxylase in the locus coeruleus of desipramine-treated rats. Neurosci. Lett. 147.

    Google Scholar 

  • Korf, J., Aghaganian, G.K. and Roth, R.H. (1973) Increased turnover of norepinephrine in the rat cerebral cortex during stress: role of locus coeruleus. Neuropsychopharmacology 12, 933-938.

    CAS  Google Scholar 

  • Kritzer, M.F. (2000) Effects of acute and chronic gonadectomy on the catecholamine innerva-tion of the cerebral cortex in adult male rats: insensitivity of axons immunoreactive for dopamine-β-hydroxylase to gonadal steroids, and differential sensitivity of axons immuno-reactive for tyrosine hydroxylase to ovarian and testicular hormones. J. Comp. Neurol. 427, 617-633.

    CAS  PubMed  Google Scholar 

  • Kritzer, M.F. (2003) Long term gonadectomy affects the density of tyrosine hydroxylase but not dopamine beta hydroxylase, choline acetyltransferase or serotonin immunoreactive axons in the medial prefrontal cortices of adult male rats. Cereb. Cortex 13, 282-296.

    CAS  PubMed  Google Scholar 

  • Krnjevic, L. and Phillips, J.W. (1963a) Iontophoretic studies of neurons in the mammalian cerebral cortex. J. Physiol. 165.

    Google Scholar 

  • Krnjevic, L. and Phillips, J.W. (1963b) Actions of certain amines on cerebral cortical neurons. Brit J Pharmacol Chemother 20, 471-490.

    CAS  Google Scholar 

  • Lapiz, M.D.S. and Morilak, D.A. (2006) Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neurosci-ence 137, 1039-1049.

    CAS  Google Scholar 

  • Law-Tho, D., Crepel, F. and Hirsch, J.C. (1993) Noradrenaline decreases transmission of NMDA- and non-NMDA-receptor mediated monosynaptic EPSPs in rat prefrontal neu-rons in vitro. Eur. J. Neurosci. 5, 1494-1500.

    CAS  PubMed  Google Scholar 

  • Levitt, P. and Moore, R.Y. (1978) Noradrenaline neuron innervation of the neocortex in the rat. Brain Res. 139, 219-231.

    CAS  PubMed  Google Scholar 

  • Lewis, D.A. and Morrison, J.H. (1989) Noradrenergic innervation of monkey prefrontal cor-tex: A dopamine-b-hydroxylase immunohistochemical study. J. Comp. Neurol. 282, 317-330.

    CAS  PubMed  Google Scholar 

  • Lewis, D.A., Foote, S.L., Goldstein, M. and Morrison, J.H. (1988) The dopaminergic innerva-tion of monkey prefrontal cortex: a tyrosine hydroxylase immunocytochemical study. Brain Res. 449, 225-243.

    CAS  PubMed  Google Scholar 

  • Lewis, D.A., Campbell, M.J., Foote, S.L., Goldstein, M. and Morrison, J.H. (1987) The distri-bution of tyrosine hydroxylase-immunoreactive fibers in primate neocortex is widespread but regionally specific. J. Neurosci. 7, 279-290.

    CAS  PubMed  Google Scholar 

  • Li, B.M. and Mei, Z.T. (1994) Delayed-response deficit induced by local injection of the alpha 2 adrenergic antagonist yohimbine into the dorsolateral prefrontal cortex in young adult monkeys. Behav. Neural Biol. 62, 134-139.

    CAS  PubMed  Google Scholar 

  • Li, B.M. and Kubota, K. (1998) Alpha-2 adrenergic modulation of prefrontal cortical neuronal activity related to a visual discrimination task with GO and NO-GO performances in mon-keys. Neurosci. Res. 31, 83-95.

    CAS  PubMed  Google Scholar 

  • Lidov, H.G.W., Rice, F.L. and Molliver, M.E. (1978) The organization of the catecholamine innervation of somatosensory cortex: the barrel field of the mouse. Brain Res. 153, 577-584.

    CAS  PubMed  Google Scholar 

  • Lindvall, O. and Björklund, A. (1984) General organization of cortical monoamine systems. In: L. Descarries, T. Reader and H. Jasper (eds.), Monoamine Innervation of the Cerebral Cortex. Liss, New York, pp. 9-40.

    Google Scholar 

  • Liprando, L.A., Miner, L.A.H., Blakely, R.D., Lewis, D.A. and Sesack, S.R. (2004) Ultra-structural interactions between terminals expressing the norepinephrine transporter and dopamine neurons in the rat and monkey ventral tegmental area. Synapse 52, 233-244.

    CAS  PubMed  Google Scholar 

  • Liu, W., Yuen, E.Y., Allen, P.B., Feng, J., Greengard, P. and Yan, Z. (2006) Adrenergic modulation of NMDA receptors in prefrontal cortex is differentially regulated by RGS proteins and spinophilin. Proc. Natl. Acad. Sci. 103, 18338-18343.

    CAS  PubMed  Google Scholar 

  • Lopez-Rubalcava, C. and Lucki, I. (2000) Strain differences in the behavioral effects of anti-depressant drugs in the forced swim test. Neuropsychopharmacology 22, 191-199.

    CAS  PubMed  Google Scholar 

  • Lorang, D., Amara, S.G. and Simerly, R.B. (1994) Cell-type-specific expression of cate-cholamine transporters in the rat brain. J. Neurosci. 14, 4903-4914.

    CAS  PubMed  Google Scholar 

  • Loughlin, S.E., Foote, S.L. and Fallon, J.H. (1982) Locus coeruleus projections to the cortex: topography, morphology and collaterization. Brain Res. Bull. 9, 287-294.

    CAS  Google Scholar 

  • Loughlin, S.E., Foote, S.L. and Bloom, F.E. (1986a) Efferent projections of nucleus locus coeruleus: topographic organization of cells of origin demonstrated by three dimensional reconstruction. Neuroscience 18, 291-306.

    CAS  PubMed  Google Scholar 

  • Loughlin, S.E., Foote, S.L. and Grzanna, R. (1986b) Efferent projections of nucleus locus coeruleus: morphologic subpopulations have different efferent targets. Neuroscience 18, 307-319.

    CAS  PubMed  Google Scholar 

  • Ma, C.L., Qi, X.L., Peng, J.Y. and Li, B.M. (2003) Selective deficit in no-go performance induced by blockade of prefrontal cortical alpha 2-adrenoceptors in monkeys. Neuroreport 14, 1013-1016.

    CAS  PubMed  Google Scholar 

  • Mamalaki, E., Kvetnansky, R., Brady, L.S., Gold, P.W. and Herkenham, M. (1992) Repeated immobilization stress alters tyrosine hydroxylase, corticotropin-releasing hormone and corticosteroid receptor messenger ribonucleic acid levels in rat brain. J. Neuroendocrinol. 4, 689-699.

    CAS  Google Scholar 

  • Mana, M.J. and Grace, A.A. (1997) Chronic cold stress alters basal and evoked electrophysio-logical activity of rat locus coeruleus neurons. Neuroscience 81, 1055-1064.

    CAS  PubMed  Google Scholar 

  • Mantz, J., Millla, C., Glowinski, J. and Thierry, A.M. (1988) Differential effects of ascending neurons containing dopamine and noradrenaline in control of spontaneous activity and of evoked responses in the rat prefrontal cortex. Neuroscience 27, 517-526.

    CAS  PubMed  Google Scholar 

  • Mao, Z.M., Arnsten, A.F. and Li, B.M. (1999) Local infusion of an alpha-1 adrenergic agonist into the prefrontal cortex impairs spatial working memory performance in monkeys. Biol. Psychiatry 46, 1259-1265.

    CAS  PubMed  Google Scholar 

  • Mason, S.T. and Figiber, H.C. (1979) Regional topography within noradrenergic locus coeruleus as revealed by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 187, 703-724.

    CAS  PubMed  Google Scholar 

  • McLean, J. and Waterhouse, B.D. (1994) Noradrenergic modulation of cat area 17 neuronal responses to moving visual stimuli. Brain Res. 667, 83-97.

    CAS  PubMed  Google Scholar 

  • McMillen, B.A., Warnack, W., German, D.C. and Shore, P.A. (1980) Effects of chronic desip-ramine treatment on rat brain noradrenergic responses to alpha-adrenergic drugs. Eur. J. Pharmacol. 61, 239-246.

    CAS  PubMed  Google Scholar 

  • Meana, J.J., Baruren, F. and Garcia-Sevilla, J.A. (1992) Alpha2-adrenoceptors in the brain of suicide victims: increased receptor density associated with major depression. Biol. Psy-chiatry 31, 471-490.

    CAS  Google Scholar 

  • Mejias-Aponte, C.A., Zhu, Y. and Aston-Jones, G. (2004) Noradrenergic innervation of mid-brain dopamine neurons: prominent inputs from A1 and A2 cell groups. Soc. Neurosci. Abstr. 465.4.

    Google Scholar 

  • Melia, K.R., Nestler, E.J. and Duman, R.S. (1992a) Chronic imipramine treatment normalizes levels of tyrosine hydroxylase in the locus coeruleus of chronically stress rats. Psy-chopharmacology 108, 23-26.

    CAS  Google Scholar 

  • Melia, K.R., Rasmussen, K., Terwilliger, R.Z., Haycock, J.W., Nestler, E.J. and Duman, R.S. (1992b) Coordinate regulation of the cyclic AMP system with firing rate and expression of tyrosine hydroxylase in the rat locus coeruleus: effects of chronic stress and drug treatment. J. Neurochem. 58, 494-502.

    CAS  PubMed  Google Scholar 

  • Melikian, H.E., Ramamoorthy, S., Tate, C.G. and Blakely, R.D. (1996) Inability to N glycosy-late the human norepinephrine transporter reduces protein stability, surface trafficking, and transport activity but not ligand recognition. Mol. Pharm. 50, 266-276.

    CAS  Google Scholar 

  • Melikian, H.E., McDonald, J.K., Gu, H., Rudnick, G., Moore, K.R. and Blakely, R.D. (1994) Human norepinephrine transporter. Biosynthetic studies using a site-directed polyclonal antibody. J. Biol. Chem. 269, 12290-12297.

    CAS  PubMed  Google Scholar 

  • Michelson, D., Adler, L., Spencer, T., Reimherr, F.W., West, S.A., Allen, A.J., Kelsey, D., Wernicke, J., Dietrich, A. and Milton, D. (2003) Atomoxetine in adults with ADHD: two randomized, placebo-controlled studies. Biol. Psychiatry 53, 112-120.

    CAS  PubMed  Google Scholar 

  • Milner, T.A. and Bacon, C.E. (1989) Ultrastructural localization of tyrosine hydroxylase-like immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 281, 479-495.

    CAS  PubMed  Google Scholar 

  • Miner, L.A.H., Schroeter, S., Blakely, R.D. and Sesack, S.R. (2000) Ultrastructural localiza-tion of the serotonin transporter in superficial and deep layers of the rat prelimbic prefron-tal cortex and its spatial relationship to dopamine terminals. J. Comp. Neurol. 427, 220-234.

    CAS  PubMed  Google Scholar 

  • Miner, L.A.H., Schroeter, S., Blakely, R.D. and Sesack, S.R. (2003) Ultrastructural localiza-tion of the norepinephrine transporter in superficial and deep layers of the rat prelimbic prefrontal cortex and its spatial relationship to probable dopamine terminals. J. Comp. Neurol. 466, 478-494.

    PubMed  Google Scholar 

  • Miner, L.A.H., Jedema, H.P., Moore, F.W., Blakely, R.D., Grace, A.A. and Sesack, S.R. (2006) Chronic stress increases the plasmalemmal distribution of the norepinephrine transporter and coexpression of tyrosine hydroxylase in norepinephrine axons in the pre-frontal cortex. J. Neurosci. 26, 1571-1578.

    CAS  PubMed  Google Scholar 

  • Moller, H.-J. (2000) Are all antidepressants the same? J. Clin. Psychiat. 61 (Suppl 10), 24-27.

    Google Scholar 

  • Molliver, M.E., Grzanna, R., Lidov, H.G.W., Morrison, J.H. and Olschowka, J.A. (1982) Monoamine systems in the cerebral cortex. In: V. Chan-Palay and S.L. Palay (eds.), Cyto-chemical Methods in Neuroanatomy. Liss, New York, pp. 255-277.

    Google Scholar 

  • Moore, H., Rose, H.J. and Grace, A.A. (2001) Chronic cold stress reduces the spontaneous activity of ventral tegmental dopamine neurons. Neuropsychopharmacology 24, 410-419.

    CAS  PubMed  Google Scholar 

  • Morrison, J.H., Molliver, M.E. and Grzanna, R. (1979) Noradrenergic innervation of cerebral cortex: widespread effects of locus cortical lesions. Science 202, 313-316.

    Google Scholar 

  • Morrison, J.H., Foote, S.L. and Bloom, F.E. (1984) Regional, laminar, developmental and functional characteristics of noradrenaline and serotonin innervation patterns in monkey cortex. In: L. Descarries, T.A. Reader and H.H. Jasper (eds.), Monoamine Innervation of Cerebral Cortex. Liss, New York, pp. 61-75.

    Google Scholar 

  • Morrison, J.H., Grzanna, R., Molliver, M.E. and Coyle, J.T. (1978) The distribution and orien-tation of noradrenergic fibers in the neocortex of the rat: an immunofluorescence study. J. Comp. Neurol. 181, 17-40.

    CAS  PubMed  Google Scholar 

  • Morrison, J.H., Molliver, M.E., Grzanna, R. and Coyle, J.T. (1981) The intracortical trajectory of the coeruleo-cortical projection in the rat: a tangentially organized afferent. Neurosci-ence 6, 139-158.

    CAS  Google Scholar 

  • Morrison, J.H., Foote, S.L., O’Conner, D. and Bloom, F.E. (1982) Laminar, tangential and regional organization of the noradrenergic innervation of monkey cortex: dopamine b-hydroxylase immunohistochemistry. Brain Res. Bull. 9, 309-319.

    CAS  Google Scholar 

  • Morruzzi, A.S. and Hart, E.R. (1955) Evoked cortical responses under the influence of hallu-cinogens and related drugs. Electroencephalgr. Clin. Neurophysiol. 1.

    Google Scholar 

  • Mostofsky, S.H., Cooper, K.L., Kates, W.R., Denckla, M.B. and Kaufmann, W.E. (2002) Smaller prefrontal and premotor volumes in boys with attention-deficit/hyperactivity dis-order. Biol. Psychiatry 52, 785-794.

    PubMed  Google Scholar 

  • Nagai, T.K., Satoh, K., Imamoto, K. and Maeda, T. (1981) Divergent projections of cate-cholamine neurons of the locus coeruleus as revealed by fluorescent retrograde double labeling technique. Neurosci. Lett. 23, 117-123.

    CAS  PubMed  Google Scholar 

  • Nelson, J.C. (1999) A review of the efficacy of serotonergic and noradrenergic reuptake in-hibitors for treatment of major depression. Biol. Psychiatry 46, 1301-1308.

    CAS  PubMed  Google Scholar 

  • Nestler, E.J., McMahon, A., Sabban, E.L., Tallman, J.F. and Duman, R.S. (1990) Chronic antidepressant administration decreases the expression of tyrosine hydroxylase in the rat locus coeruleus. Proc. Natl. Acad. Sci. 87, 7522-7526.

    CAS  PubMed  Google Scholar 

  • Nicholas, A.P., Pieribone, V.A. and Hokfelt, T. (1993a) Cellular localization of messenger RNA for beta-1 and beta-2 adrenergic receptors in rat brain: an in situ hybridization study. Neuroscience 56, 1023-1039.

    CAS  PubMed  Google Scholar 

  • Nicholas, A.P., Pieribone, V. and Holkfelt, T. (1993b) Distribution of mRNA for alpha2-adrenergic receptor subtypes in rat brain: an in situ hybridization study. J. Comp. Neurol. 328, 575-594.

    CAS  PubMed  Google Scholar 

  • Nirenberg, M.J., Vaughan, R.A., Uhl, G.R., Kuhar, M.J. and Pickel, V.M. (1996) The dopa-mine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16, 436-447.

    CAS  PubMed  Google Scholar 

  • Nisenbaum, L.K., Zigmond, M.J., Sved, A.F. and Abercrombie, E.D. (1991) Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor. J. Neurosci. 11, 1478-1484.

    CAS  PubMed  Google Scholar 

  • Noack, H.J. and Lewis, D.A. (1989) Antibodies directed against tyrosine hydroxylase differ-entially recognize noradrenergic axons in monkey neocortex. Brain Res. 500, 313-324.

    CAS  PubMed  Google Scholar 

  • Nutt, D.J., Lalies, M.D., Lione, L.A. and Hudson, A.L. (1997) Noradrenergic mechanisms in the prefrontal cortex. J. Psychopharmacol. 11, 163-168.

    CAS  PubMed  Google Scholar 

  • Olschowka, J.A., Molliver, M.E., Grzanna, R., Rice, F.L. and Coyle, J.T. (1981) Ultrastruc-tural demonstration of noradrenergic synapses in the rat central nervous system by dopa-mine-b-hydroxylase immunocytochemistry. J. Histochem. Cytochem. 29, 271-280.

    CAS  PubMed  Google Scholar 

  • Ossowska, G., Nowak, G., Kata, R., Klenk-Majewska, B., Canilczuk, Z. and Zebrowska-Lupina, I. (2001) Brain monoamine receptors in a chronic unpredictable stress model in rats. J. Neural Transm. 108, 311-319.

    CAS  PubMed  Google Scholar 

  • Page, M.E. and Lucki, I. (2002) Effects of acute and chronic reboxetine treatment on stress-induced monoamine efflux in the rat frontal cortex. Neuropsychopharmacology 27, 237-247.

    CAS  PubMed  Google Scholar 

  • Palacios, J.M. and Kuhar, M.J. (1980) Beta-adrenergic-receptor localization by light micro-scopic autoradiography. Science 208, 1378-1380.

    CAS  PubMed  Google Scholar 

  • Palacios, J.M. and Kuhar, M.J. (1982) Beta-adrenergic receptor localization by light micro-scopic autoradiography. Neurochem. Int. 4, 473-490.

    CAS  PubMed  Google Scholar 

  • Palacios, J.M. and Wamsley, J.K. (1983) Microscopic localization of adrenoreceptors. In: G. Kinos (ed.), Adrenoreceptors and Catecholamine Action, Part B. Wiley, New York, pp. 295-313.

    Google Scholar 

  • Palacios, J.M. and Wamsley, J.K. (1984) Catecholamine receptors. In: A. Bjorklund, T. Hok-felt and M.J. Kuhar (eds.), Handbook of Chemical Neuroanatomy, Vol. 3.: Classical Transmitters and Transmitter Receptors in the CNS, Part II. Elsevier, New York, pp. 325-351.

    Google Scholar 

  • Papadopoulos, G., Parnavelas, J. and Bujis, R. (1989) Light and electron microscopic immu-nocytochemical analysis of the noradrenaline innervation of the rat visual cortex. J. Neurocytol. 18, 1-10.

    CAS  PubMed  Google Scholar 

  • Papadopoulos, G.C. and Parnavelas, J.G. (1991) Monoamine systems in the cerebral cortex: evidence for anatomical specificity. Prog. Neurobiol. 36, 195-200.

    CAS  PubMed  Google Scholar 

  • Papp, M., Moryl, E. and Wilner, P. (1996) Pharmacological validation of the chronic mild stress model of depression. Eur. J. Pharmacol. 296, 129-136.

    CAS  PubMed  Google Scholar 

  • Pardon, M.-C., Gould, G.G., Garcia, A., Phillips, L., Cook, M.C., Miller, S.A., Mason, P.A. and Morilak, D.A. (2002) Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115, 229-242.

    CAS  PubMed  Google Scholar 

  • Pare, W.P. (1994) Open field, learned helplessness, defensive burying and forced-swim test in WKY rats. Physiol. Behav. 55, 433-439.

    CAS  PubMed  Google Scholar 

  • Parnavelas, J., Moises, H. and Speciale, S. (1985) The monoaminergic innervation of the rat visual cortex. Proc. Royal Soc. Lond. 223, 319-329.

    CAS  Google Scholar 

  • Pavcovich, L.A. and Ramirez, O.A. (1991) Time course of uncontrollable stress in locus coeruleus neuronal activity. Brain Res. Bull. 26, 17-21.

    CAS  Google Scholar 

  • Pickel, V.M., Segal, M. and Bloom, F.E. (1974) A radioautographic study of the efferent pathways of the nucleus locus coeruleus. J. Comp. Neurol. 155, 15-42.

    CAS  PubMed  Google Scholar 

  • Pickel, V.M., Joh, T.H. and Reis, D.J. (1975a) Ultrastructural localization of tyrosine hydroxy-lase in noradrenergic neurons of brain. Proc. Natl. Acad. Sci. 72, 659-663.

    CAS  PubMed  Google Scholar 

  • Pickel, V.M., Joh, T.H. and Reis, D.J. (1975b) Immunohistochemical localization of tyrosine hydroxylase in brain by light and electron microscopy. Brain Res. 85, 295-300.

    CAS  PubMed  Google Scholar 

  • Pickel, V.M., Joh, T.H., Field, P.M., Becker, C.G. and Reis, D.J. (1975c) Cellular localization of tyrosine hydroxylase by immunocytochemistry. J. Histochem. Cytochem. 23, 1-12.

    CAS  PubMed  Google Scholar 

  • Pliszka, S.R., McCracken, J.T. and Maas, J.W. (1996) Catecholamines in attention-deficit hyperactivity disorder: current prospectives. J. Am. Acad. Child Adolesc. Psychiatry 35, 264-272.

    CAS  PubMed  Google Scholar 

  • Raiteri, M., Del Carmine, R., Bertollini, A. and Levi, G. (1977) Effect of sympathomimetic amines on the synaptosomal transport of noradrenaline, dopamine and 5-hydroxytrypt-amine. Eur. J. Pharmacol. 41, 133-143.

    CAS  PubMed  Google Scholar 

  • Rauch, S.L., Shin, L.M., Segal, E., Pitman, R.K., Carson, M.A., McMullin, K., Whalen, P.J. and Makris, N. (2003) Selectively reduced regional cortical volumes in post-traumatic stress disorder. Neuroreport 14, 913-916.

    PubMed  Google Scholar 

  • Reader, T., Ferron, A., Descarries, L. and Jasper, H. (1979) Modulatory role for biogenic amines in the cerebral cortex. Microiontophoretic studies. Brain Res. 160, 217-229.

    CAS  PubMed  Google Scholar 

  • Ren, Z.G., Porzgen, P., Zhang, J.M., Chen, X.R., Amara, S.G., Blakely, R.D. and Sieber-Blum, M. (2001) Autocrine regulation of norepinephrine transporter expression. Mol. Cell. Neurosci. 17, 539-550.

    CAS  PubMed  Google Scholar 

  • Rex, A., Sondern, U., Voight, J.P., Franck, S. and Fink, H. (1996) Strain differences in fear-motivated behavior of rats. Pharmacol. Biochem. Behav. 54, 107-111.

    CAS  PubMed  Google Scholar 

  • Robbins, T.W. (1984) Cortical noradrenaline, attention and arousal. Psychol. Med. 14, 13-21.

    CAS  PubMed  Google Scholar 

  • Room, P., Postema, F. and Korf, J. (1981) Divergent axon collaterals of rat locus coeruleus neurons: demonstration by a fluorescent double labeling technique. Brain Res. 221.

    Google Scholar 

  • Rosario, L.A. and Abercrombie, E.D. (1999) Individual differences in behavioral reactivity: correlation with stress-induced norepinephrine efflux in the hippocampus of Sprague-Dawley rats. Brain Res. Bull. 48, 595-602.

    CAS  Google Scholar 

  • Rossetti, Z.L., Pani, L., Portas, C. and Gessa, G. (1989) Brain dialysis provides evidence for D2-dopamine receptors modulating noradrenaline release in the rat frontal cortex. Eur. J. Pharmacol. 163, 393-395.

    CAS  PubMed  Google Scholar 

  • Rusnak, M., Zorad, S., Buckendahl, P., Sabban, E.L. and Kvetnansky, R. (1998) Tyrosine hydroxylase mRNA levels in locus coeruleus of rats during adaption to long-term immobi-lization stress exposure. Mol. Chem. Neuropath. 33, 249-258.

    CAS  Google Scholar 

  • Russell, V., Allie, S. and Wiggins, T. (2000) Increased noradrenergic activity in prefrontal cortex slices of an animal model for attention-deficit hyperactivity disorder - the sponta-neously hypertensive rat. Behav. Brain Res. 117, 69-74.

    CAS  PubMed  Google Scholar 

  • Sacchetti, G., Bernini, M., Bianchetti, A., Parini, S., Invernizzi, R.M. and Samanin, R. (1999) Studies on the acute and chronic effects of reboxetine on extracellular noradrenaline and other monoamines in the rat brain. Br. J. Pharmacol. 128, 1332-1338.

    CAS  PubMed  Google Scholar 

  • Savchenko, V., Sung, U. and Blakely, R.D. (2003) Cell surface trafficking of the antidepres-sant-sensitive norepinephrine transporter revealed with an ectodomain antibody. Mol. Cell. Neurosci. 24, 1131-1150.

    CAS  PubMed  Google Scholar 

  • Sawaguchi, T. (1998) Attenuation of delay-period activity of monkey prefrontal neurons by an alpha2-adrenergic antagonist during an oculomotor delayed-response task. J. Neuro-physiol. 80, 2200-2205.

    CAS  Google Scholar 

  • Sawaguchi, T. and Matsumura, M. (1985) Laminar distribution of neurons sensitive to acetyl-choline, noradrenaline and dopamine in the dorsolateral prefrontal cortex of the monkey. Neurosci. Res. 2, 255-273.

    CAS  PubMed  Google Scholar 

  • Schmidt, R.H. and Bhatnagar, R.K. (1979) Assessment of the effects of neonatal subcutaneous 6-hydroxydopamine on noradrenergic and dopaminergic innervation of the cerebral cor-tex. Brain Res. 166, 309-319.

    CAS  PubMed  Google Scholar 

  • Schroeter, S., Apparsundaram, S., Wiley, R.G., Miner, L.A.H., Sesack, S.R. and Blakely, R.D. (2000) Immunolocalization of the cocaine- and antidepressant-sensitive 1-norepinephrine transporter. J. Comp. Neurol. 420, 211-232.

    CAS  PubMed  Google Scholar 

  • Séguéla, P., Watkins, K.C. and Descarries, L. (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat. Brain Res. 442, 11-22.

    PubMed  Google Scholar 

  • Séguéla, P., Watkins, K.C. and Descarries, L. (1989) Ultrastructural relationships of serotonin axon terminals in the cerebral cortex of the adult rat. J. Comp. Neurol. 289, 129-142.

    PubMed  Google Scholar 

  • Séguéla, P., Watkins, K.C., Geffard, M. and Descarries, L. (1990) Noradrenaline axon termi-nals in adult rat neocortex: an immunocytochemical analysis in serial thin sections. Neuro-science 35, 249-264.

    Google Scholar 

  • Sesack, S.R., Snyder, C.L. and Lewis, D.A. (1995) Axon terminals immunolabeled for dopa-mine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J. Comp. Neurol. 363, 264-280.

    CAS  PubMed  Google Scholar 

  • Sesack, S.R., Miner, L.A.H. and Omelchenko, N. (2006) Pre-embedding immunoelectron microscopy: applications for studies of the nervous system. In: L. Zaborszky, F.G. Wouterlood and J.L. Lanciego (eds.), Neuroanatomical Tract-Tracing 3: Molecules, Neu-rons, Systems. Springer, New York, pp. 6-71.

    Google Scholar 

  • Sesack, S.R., Hawrylak, V.A., Matus, C., Guido, M.A. and Levey, A.I. (1998) Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunore-activity for the dopamine transporter. J. Neurosci. 18, 2697-2708.

    CAS  PubMed  Google Scholar 

  • Shin, L.M., Whalen, P.J., Pitman, R.K., Bush, G., Macklin, M.l., Lasko, N.B., Orr, S.P., McInerney, S.C. and Rauch, S.L. (2001) An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol. Psychiatry 50, 932-942.

    CAS  PubMed  Google Scholar 

  • Shores, M.M., Szot, P. and Veith, R.C. (1994) Desipramine-induced increase in norepineph-rine transporter mRNA is not mediated via alpha2 receptors. Molec. Brain Res. 27, 337-341.

    CAS  PubMed  Google Scholar 

  • Simpson, K.L., Waterhouse, B.D. and Lin, R.C. (2006) Characterization of neurochemically specific projections from the locus coeruleus with respect to somatosensory-related bar-rels. Anat. Rec. Part A 288A, 166-173.

    CAS  Google Scholar 

  • Simpson, K.L., Altman, D.W., Wang, L., Kirifides, M.L., Lin, R.C. and Waterhouse, B.D. (1997) Lateralization and functional organization of the locus coeruleus projection to the trigeminal somatosensory pathway in rat. J. Comp. Neurol. 385, 135-147.

    CAS  PubMed  Google Scholar 

  • Simson, P.E. and Weiss, J.M. (1988) Altered activity of the locus coeruleus in an animal model of depression. Neuropsychopharmacology 1, 287-294.

    CAS  PubMed  Google Scholar 

  • Soares, J.C. and Mann, J.J. (1997) The functional neuroanatomy of mood disorders. J. Psychi-atric Res. 31, 393-432.

    CAS  Google Scholar 

  • Solanto, M.V. (1998) Neuropsychopharmacological mechanisms of stimulant drug action in attention-deficit hyperactivity disorder: a review and integration. Behav. Brain Res. 94, 127-152.

    CAS  PubMed  Google Scholar 

  • Southwick, S.M., Bremner, J.D., Rasmusson, A., Morgan, D.A., Arnsten, A.F.T. and Charney, D.S. (1999) Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol. Psychiatry 46, 1192-1204.

    CAS  PubMed  Google Scholar 

  • Southwick, S.M., Krystal, J.H., Morgan, C.A., Johnson, D.R., Nagy, L.M., Nicolaou, A., Heninger, G.R. and Charney, D. (1993) Abnormal noradrenergic function in posttraumatic stress disorder. Arch. Gen. Psychiatry 50, 266-274.

    CAS  PubMed  Google Scholar 

  • Spencer, T., Biederman, J., Coffey, B., Geller, D., Crawford, M., Bearman, S.K., Tarazi, B. and Faraone, S.V. (2002) A double-blind comparison of desipramine and placebo in children and adolescents with chronic Tic disorder and comorbid attention-deficit/ hyperactivity disorder. Arch. Gen. Psychiatry 59, 649-656.

    CAS  PubMed  Google Scholar 

  • Stanford, S.C. (1995) Central noradrenergic neurons and stress. Pharmacol Therapeutics 68, 297-242.

    CAS  Google Scholar 

  • Steindler, D.A. (1981) Locus coeruleus neurons have axons that branch to the forebrain and cerebellum. Brain Res. 223, 367-373.

    CAS  PubMed  Google Scholar 

  • Stone, E.A., Freedman, L.S. and Morgano, L.E. (1978) Brain and adrenal tyrosine hydroxylase activity after chronic footshock stress. Pharmacol. Biochem. Behav. 9, 551-553.

    CAS  PubMed  Google Scholar 

  • Sung, U., Apparsundaram, S., Galli, A., Kahlig, K.M., Savchenko, V., Schroeter, S., Quick, M.W. and Blakely, R.D. (2003) A regulated interaction of syntaxin 1A with the antidepressant-sensitive norepinephrine transporter establishes catecholamine clearance capacity. J. Neurosci. 23, 1697-1709.

    CAS  PubMed  Google Scholar 

  • Svensson, T.H. and Udin, T. (1978) Feedback inhibition of brain noradrenaline neurons by tricyclic antidepressants: alpha-receptor mediation. Science 202, 1089-1091.

    CAS  PubMed  Google Scholar 

  • Swanson, L.W. and Hartman, B.K. (1975) The central adrenergic system. An immunofluores-cence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-B-hydroxylase as a marker. J. Comp. Neurol. 163, 467-487.

    CAS  PubMed  Google Scholar 

  • Szabo, S.T. and Blier, P. (2001) Effect of the selective noradrenergic reuptake inhibitor re-boxetine on the firing activity of noradrenaline and serotonin neurons. Eur. J. Neurosci. 13, 2077-2087.

    CAS  PubMed  Google Scholar 

  • Szot, P., Ashliegh, E.A., Kohen, R., Petrie, E., Dorsa, D.M. and Veith, R. (1993) Norepineph-rine transporter mRNA is elevated in the locus coeruleus following short- and long-term desipramine treatment. Brain Res. 618, 308-312.

    CAS  PubMed  Google Scholar 

  • Tanda, G., Pontier, F.E., Frau, R. and DiChiara, G. (1997) Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine. Eur. J. Neurosci. 9, 2077-2085.

    CAS  PubMed  Google Scholar 

  • Tanda, G.L., Carboni, E., Frau, R. and DiChiara, G. (1994) Increase of extracellular dopamine in the prefrontal cortex: portrait of drugs with antidepressant potential? Psychopharma-cology 115, 285-288.

    CAS  Google Scholar 

  • Tanila, H., Rama, P. and Carlson, S. (1996) The effects of prefrontal intracortical microinjec-tions of an alpha-2 agonist, alpha-2 antagonist and lidocaine on the delayed alternation performance of aged rats. Brain Res. Bull. 40, 117-119.

    CAS  Google Scholar 

  • Tejani-Butt, S.M., Pare, W.P. and Yang, J. (1994) Effect of repeated novel stressors on de-pressive behavior and brain norepinephrine receptor system in Sprague-Dawley and Wistar Kyoto (WKY) rats. Brain Res. 649, 27-35.

    CAS  PubMed  Google Scholar 

  • Tillet, Y. and Kitahama, K. (1998) Distribution of central catecholaminergic neurons: a com-parison between ungulates, humans and other species. Histol. Histopathol. 13, 1163-1177.

    CAS  PubMed  Google Scholar 

  • Ungerstedt, U. (1971) Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol. Scand. 367 [Suppl.], 1-48.

    CAS  Google Scholar 

  • Van Dengen, P. (1981) The central norepinephrine transmission and the locus coeruleus: a review of the data. Prog. Neurobiol. 16, 117-143.

    Google Scholar 

  • Venkatesan, C., Song, X.Z., Go, C.G., Kurose, H. and Aoki, C. (1996) Cellular and subcellu-lar distribution of a 2A -adrenergic receptors in the visual cortex of neonatal and adult rats. J. Comp. Neurol. 365, 79-95.

    CAS  PubMed  Google Scholar 

  • Verhofstad, A.A., Hokfelt, T., Goldstein, M., Steinbusch, H.W. and Joosten, H.W. (1979) Appearance of tyrosine hydroxylase, aromatic amino-acid decarboxylase, dopamine beta-hydroxylase and phenylethanolamine N-methyltransferase during the ontogenesis of the adrenal medulla: an immunohistochemical study in the rat. Cell Tiss. Res. 200, 1-13.

    CAS  Google Scholar 

  • Vos, P., Kaufmann, D., Hand, P.J. and Wolfe, B.B. (1990) Beta 2-adrenergic receptors are colocalized and coregulated with “whisker barrels” in rat somatosensory cortex. Proc. Natl. Acad. Sci. 87, 5114-5118.

    CAS  PubMed  Google Scholar 

  • Wamsley, J.K. (1984) Autoradiographic localization of cortical biogenic amine receptors. In: L. Descarries, T.A. Reader and H.H. Jasper (eds.), Monoamine Innervation of Cerebral Cortex. Liss, New York, pp. 153-174.

    Google Scholar 

  • Wamsley, J.K., Palacios, J.M., Young, W.S. and Kuhar, M.J. (1981) Autoradiographic deter-mination of neurotransmitter receptor distributions in the cerebral and cerebellar cortices. J. Histochem. Cytochem. 29, 125-135.

    CAS  PubMed  Google Scholar 

  • Wang, M., Tang, Z.X. and Li, B.M. (2004) Enhanced visuomotor associative learning follow-ing stimulation of alpha 2A-adrenoceptors in the ventral prefrontal cortex in monkeys. Brain Res. 1024, 176-182.

    CAS  PubMed  Google Scholar 

  • Wang, P., Kitayama, I. and Nomura, J. (1998) Tyrosine hydroxylase gene expression in the locus coeruleus of depression-model rats and rats exposed to short- and long-term forced walking stress. Life Sci. 62, 2083-8092.

    CAS  PubMed  Google Scholar 

  • Watanabe, Y., McKittrick, C.R., Blanchard, D.C., Blanchard, R.J., McEwen, B.S. and Sakai, R.R. (1995) Effects of chronic social stress on tyrosine hydroxylase mRNA and protein levels. Molec. Brain Res. 32, 176-180.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B., Lin, C., Burne, R. and Woodward, D. (1983) The distribution of neocortical projection neurons in the locus coeruleus. J. Comp. Neurol. 217, 418-431.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B.D. and Woodward, D.J. (1980) Interaction of norepinephrine with cerebrocor-tical activity evoked by stimulation of somatosensory afferent pathways in the rat. Exp. Neurol. 67, 11-34.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B.D., Moises, H.C. and Woodward, D.J. (1980) Noradrenergic modulation of somatosensory cortical neuronal responses to iontophoretically applied putative neuro-transmitters. Exp. Neurol. 69, 30-49.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B.D., Moises, H.C. and Woodward, D.J. (1981) Alpha receptor mediated facilita-tion of somatosensory cortical neuronal responses to excitatory synaptic inputs and ionto-phoretically applied acetylcholine. Neuropharmacology 20, 907-920.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B.D., Moises, H.C. and Woodward, D.J. (1982) Norepinephrine enhancement of inhibitory synaptic mechanisms in cerebellum and cerebral cortex: mediation by beta adrenergic receptors. J. Pharm. Exp. Ther. 221, 495-506.

    CAS  Google Scholar 

  • Waterhouse, B.D., Moises, H.C. and Woodward, D.J. (1998) Phasic activation of the locus coeruleus enhances responses of primary sensory cortical neurons to peripheral receptive field stimulation. Brain Res. 790, 33-44.

    CAS  PubMed  Google Scholar 

  • Waterhouse, B.D., Azizi, S.A., Burne, R.A. and Woodward, D.J. (1988) New evidence for a gating action of norepinephrine in central neuronal circuits of mammalian brain. Brain Res. Bull. 21, 425-432.

    CAS  Google Scholar 

  • Waterhouse, B.D., Azizi, S.A., Burne, R.A. and Woodward, D.J. (1990) Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis. Brain Res. 514, 276-292.

    CAS  PubMed  Google Scholar 

  • Weinshenker, D., White, S.S., Javors, M.A., Palmiter, R.D. and Szot, P. (2002) Regulation of the norepinephrine transporter abundance by catecholamines and desipramine in vivo. Brain Res. 946, 239-246.

    CAS  PubMed  Google Scholar 

  • Yamamoto, B.K. and Novotney, S. (1998) Regulation of extracellular dopamine by the nore-pinephrine transporter. J. Neurochem. 71, 274-280.

    Article  CAS  PubMed  Google Scholar 

  • Young, W.S. and Kuhar, M.J. (1980) Noradrenergic a1 and a2 receptors: light microscopic autoradiographic localization. Proc. Natl. Acad. Sci. 77, 1696-1700.

    CAS  PubMed  Google Scholar 

  • Zametkin, A.J., Nordahl, T.E., Gross, M., King, A.C., Semple, W.E., Rumsey, J., Hamburger, S. and Cohen, R.M. (1990) Cerebral glucose metabolism in adults with hyperactivity of childhood onset. N. Engl. J. Med. 323, 1361-1366.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, M.-Y., Kim, C.-H., Hwang, D.-Y., Baldessarini, R. and Kim, K.-S. (2002) Effects of desipramine treatment on norepinephrine transporter gene expression in the cultured SK-N-BE(2)M17 cells and rat brain tissue. J. Neurochem. 82, 146-153.

    CAS  PubMed  Google Scholar 

  • Zhu, M.-Y., Klimek, V., Dilley, G.E., Haycock, J.W., Stockmeier, C., Overholser, J.C., Melt-zer, H.Y. and Ordway, G.A. (1999) Elevated levels of tyrosine hydroxylase in the locus coeruleus in major depression. Biol. Psychiatry 46, 1275-1286.

    CAS  PubMed  Google Scholar 

  • Zigmond, M.J., Finlay, J.M. and Sved, A.F. (1995) Neurochemical studies of central noradrenergic responses to acute and chronic stress. In: M.J. Friedman, D.S. Charney and A.Y. Deutsch (eds.), Neurobiological and Clinical Consequences of Stress: From Normal Adaptations to PTSD. Lippencott-Raven, Philadelphia, pp. 45-60.

    Google Scholar 

  • Zigmond, R.E., Schon, F. and Iversen, L.L. (1974) Increased tyrosine hydroxylase activity in the locus coeruleus of rat brain after reserpine treatment and cold stress. Brain Res. 70, 547-552.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Miner, L.A.H., Sesack, S.R. (2007). Anatomical Characteristics of Norepinephrine Axons in the Prefrontal Cortex: Unexpected Findings That May Indicate Low Activity State in Naïve Animals. In: Tseng, KY., Atzori, M. (eds) Monoaminergic Modulation of Cortical Excitability. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-72256-6_3

Download citation

Publish with us

Policies and ethics