Activation of dopamine neurons is critical for aversive conditioning and prevention of generalized anxiety (original) (raw)

References

  1. Wise, R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483–494 (2004).
    Article CAS Google Scholar
  2. Mantz, J., Thierry, A.M. & Glowinski, J. Effect of noxious tail pinch on the discharge rate of mesocortical and mesolimbic dopamine neurons: selective activation of the mesocortical system. Brain Res. 476, 377–381 (1989).
    Article CAS PubMed Google Scholar
  3. Ungless, M.A., Magill, P.J. & Bolam, J.P. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303, 2040–2042 (2004).
    Article CAS PubMed Google Scholar
  4. Brischoux, F., Chakraborty, S., Brierley, D.I. & Ungless, M.A. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc. Natl. Acad. Sci. USA 106, 4894–4899 (2009).
    Article CAS PubMed Google Scholar
  5. Chiodo, L.A., Caggiula, A.R., Antelman, S.M. & Lineberry, C.G. Reciprocal influences of activating and immobilizing stimuli on the activity of nigrostriatal dopamine neurons. Brain Res. 176, 385–390 (1979).
    Article CAS PubMed Google Scholar
  6. Joshua, M., Adler, A., Mitelman, R., Vaadia, E. & Bergman, H. Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J. Neurosci. 28, 11673–11684 (2008).
    Article CAS Google Scholar
  7. Matsumoto, M. & Hikosaka, O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837–841 (2009).
    Article CAS PubMed Google Scholar
  8. Schultz, W. & Romo, R. Responses of nigrostriatal dopamine neurons to high-intensity somatosensory stimulation in the anesthetized monkey. J. Neurophysiol. 57, 201–217 (1987).
    Article CAS PubMed Google Scholar
  9. Bromberg-Martin, E.S., Matsumoto, M. & Hikosaka, O. Dopamine in motivational control: rewarding, aversive and alerting. Neuron 68, 815–834 (2010).
    Article CAS PubMed Google Scholar
  10. Lovibond, P.F. & Shanks, D.R. The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. J. Exp. Psychol. Anim. Behav. Process. 28, 3–26 (2002).
    Article PubMed Google Scholar
  11. Grillon, C. Associative learning deficits increase symptoms of anxiety in humans. Biol. Psychiatry 51, 851–858 (2002).
    Article PubMed Google Scholar
  12. Pezze, M.A. & Feldon, J. Mesolimbic dopaminergic pathways in fear conditioning. Prog. Neurobiol. 74, 301–320 (2004).
    Article CAS PubMed Google Scholar
  13. Komendantov, A.O., Komendantova, O.G., Johnson, S.W. & Canavier, C.C. A modeling study suggests complementary roles for GABAA and NMDA receptors and the SK channel in regulating the firing pattern in midbrain dopamine neurons. J. Neurophysiol. 91, 346–357 (2004).
    Article CAS PubMed Google Scholar
  14. Overton, P. & Clark, D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 10, 131–140 (1992).
    Article CAS PubMed Google Scholar
  15. Overton, P.G. & Clark, D. Burst firing in midbrain dopaminergic neurons. Brain Res. Brain Res. Rev. 25, 312–334 (1997).
    Article CAS PubMed Google Scholar
  16. Zweifel, L.S. et al. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. USA 106, 7281–7288 (2009).
    Article CAS PubMed Google Scholar
  17. Zweifel, L.S., Argilli, E., Bonci, A. & Palmiter, R.D. Role of NMDA receptors in dopamine neurons for plasticity and addictive behaviors. Neuron 59, 486–496 (2008).
    Article CAS PubMed Google Scholar
  18. Robinson, S., Smith, D.M., Mizumori, S.J. & Palmiter, R.D. Firing properties of dopamine neurons in freely moving dopamine-deficient mice: effects of dopamine receptor activation and anesthesia. Proc. Natl. Acad. Sci. USA 101, 13329–13334 (2004).
    Article CAS PubMed Google Scholar
  19. Chiodo, L.A., Antelman, S.M., Caggiula, A.R. & Lineberry, C.G. Sensory stimuli alter the discharge rate of dopamine (DA) neurons: evidence for two functional types of DA cells in the substantia nigra. Brain Res. 189, 544–549 (1980).
    Article CAS PubMed Google Scholar
  20. Margolis, E.B., Lock, H., Hjelmstad, G.O. & Fields, H.L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J. Physiol. (Lond.) 577, 907–924 (2006).
    Article CAS Google Scholar
  21. Luo, A.H., Georges, F.E. & Aston-Jones, G.S. Novel neurons in ventral tegmental area fire selectively during the active phase of the diurnal cycle. Eur. J. Neurosci. 27, 408–422 (2008).
    Article PubMed Google Scholar
  22. Davis, M., Falls, W.A., Campeau, S. & Kim, M. Fear-potentiated startle: a neural and pharmacological analysis. Behav. Brain Res. 58, 175–198 (1993).
    Article CAS PubMed Google Scholar
  23. Fadok, J.P., Dickerson, T.M. & Palmiter, R.D. Dopamine is necessary for cue-dependent fear conditioning. J. Neurosci. 29, 11089–11097 (2009).
    Article CAS PubMed Google Scholar
  24. Richardson, R. Shock sensitization of startle: learned or unlearned fear? Behav. Brain Res. 110, 109–117 (2000).
    Article CAS PubMed Google Scholar
  25. Grillon, C. Startle reactivity and anxiety disorders: aversive conditioning, context and neurobiology. Biol. Psychiatry 52, 958–975 (2002).
    Article PubMed Google Scholar
  26. Koch, M. & Schnitzler, H.U. The acoustic startle response in rats—circuits mediating evocation, inhibition and potentiation. Behav. Brain Res. 89, 35–49 (1997).
    Article CAS PubMed Google Scholar
  27. Hunter, A.J., Nolan, P.M. & Brown, S.D. Towards new models of disease and physiology in the neurosciences: the role of induced and naturally occurring mutations. Hum. Mol. Genet. 9, 893–900 (2000).
    Article CAS PubMed Google Scholar
  28. Ralph, R.J. et al. The dopamine D2, but not D3 or D4, receptor subtype is essential for the disruption of prepulse inhibition produced by amphetamine in mice. J. Neurosci. 19, 4627–4633 (1999).
    Article CAS PubMed Google Scholar
  29. Grillon, C. et al. Cortisol and DHEA-S are associated with startle potentiation during aversive conditioning in humans. Psychopharmacology (Berl.) 186, 434–441 (2006).
    Article CAS Google Scholar
  30. Jovanovic, T. et al. Fear potentiation is associated with hypothalamic-pituitary-adrenal axis function in PTSD. Psychoneuroendocrinology 35, 846–857 (2010).
    Article CAS PubMed Google Scholar
  31. Sánchez, M.M. et al. Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biol. Psychiatry 57, 373–381 (2005).
    Article PubMed Google Scholar
  32. Flood, D.G., Zuvich, E., Marino, M.J. & Gasior, M. The effects of d-amphetamine, methylphenidate, sydnocarb and caffeine on prepulse inhibition of the startle reflex in DBA/2 mice. Psychopharmacology (Berl.) 211, 325–336 (2010).
    Article CAS Google Scholar
  33. Ungless, M.A., Whistler, J.L., Malenka, R.C. & Bonci, A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583–587 (2001).
    Article CAS Google Scholar
  34. Lammel, S. et al. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57, 760–773 (2008).
    Article CAS PubMed Google Scholar
  35. LeDoux, J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000).
    Article CAS Google Scholar
  36. Swerdlow, N.R. et al. Toward understanding the biology of a complex phenotype: rat strain and substrain differences in the sensorimotor gating-disruptive effects of dopamine agonists. J. Neurosci. 20, 4325–4336 (2000).
    Article CAS PubMed Google Scholar
  37. Paxinos, G. & Franklin, K.B.J. The Mouse Brain in Stereotaxic Coordinates (Academic Press, San Diego, California, 2001)

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