Letter | Published:

Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning

Abstract

Pavlovian conditioning results when an innocuous stimulus, such as an odour, is paired with a behaviourally relevant stimulus, such as a foot-shock, so that eventually the former stimulus alone will elicit the behavioural response of the latter. The lateral nucleus of the amygdala (LAT) is necessary for the emotional memory formation in this paradigm1,2,3,4. Enhanced neuronal firing in LAT to conditioned stimuli emerge in parallel with the behavioural changes5,6,7,8,9,10,11 and are dependent on local dopamine12,13,14,15. To study the changes in neuronal excitability and synaptic drive that contribute to the pavlovian conditioning process, here we used in vivo intracellular recordings to examine LAT neurons during pavlovian conditioning in rats. We found that repeated pairings of an odour with a foot-shock resulted in enhanced post-synaptic potential (PSP) responses to the odour and increased neuronal excitability. However, a non-paired odour displayed PSP decrement. The dopamine antagonist haloperidol blocked the PSP enhancement and associated increased neuronal excitability, without reversing previous conditioning. These results demonstrate that conditioning and habituation processes produce opposite effects on LAT neurons and that dopamine is important in these events, consistent with its role in emotional memory formation.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Maren, S. Long-term potentiation in the amygdala: a mechanism for emotional learning and memory. Trends Neurosci. 22, 561–567 (1999)

  2. 2

    Davis, M., Rainnie, D. & Cassell, M. Neurotransmission in rat amygdala related to fear and anxiety. Trends Neurosci. 17, 208–214 (1994)

  3. 3

    Cousens, G. & Otto, T. Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behav. Neurosci. 112, 1092–1103 (1998)

  4. 4

    Faneslow, M. S. & LeDoux, J. E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23, 229–232 (1999)

  5. 5

    Ben-Ari, Y. & Le Gal La Salle, G. Plasticity at the unitary level. II. Modifications during sensory-related association procedures. Electroencephalogr. Clin. Neurophysiol. 32, 667–679 (1972)

  6. 6

    Maren, S., Poremba, A. & Gabriel, M. Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain Res. 549, 311–316 (1991)

  7. 7

    Rogan, M. T., Staubli, U. V. & LeDoux, J. E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604–607 (1997)

  8. 8

    Nishijo, H., Uwano, T., Tamura, R. & Ono, T. Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J. Neurophys. 79, 21–36 (1998)

  9. 9

    Pare, D. & Collins, D. R. Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J. Neurosci. 20, 2701–2710 (2000)

  10. 10

    Collins, D. R. & Pare, D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS+ and CS - . Learn. Mem. 7, 97–103 (2000)

  11. 11

    Repa, J. C. et al. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nature Neurosci. 4, 724–731 (2001)

  12. 12

    Guarraci, F. A., Frohardt, R. J. & Kapp, B. S. Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res. 827, 28–40 (1999)

  13. 13

    Guarraci, F. A., Frohardt, R. J., Falls, W. A. & Kapp, B. S. The effects of intraamygdaloid infusions of a D2 dopamine receptor antagonist on Pavlovian fear conditioning. Behav. Neurosci. 114, 647–651 (2000)

  14. 14

    Greba, Q. & Kokkinidis, L. Peripheral and intraamygdalar administration of the dopamine D1 receptor antagonist SCH23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle. Behav. Neurosci. 114 2, 262–272 (2001)

  15. 15

    Greba, Q., Gifkins, A. & Kokkinidis, L. Inhibition of amygdaloid dapamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res. 899, 218–226 (2001)

  16. 16

    Rescorla, R. A. Pavlovian conditioning and its proper control procedures. Psychol. Rev. 74 1, 71–80 (1967)

  17. 17

    Dutton, R. C. et al. The concentration of isoflurane required to suppress learning depends on the type of learning. Anesthesiology 94, 514–519 (2001)

  18. 18

    Gold, P. E., Weinberger, N. M. & Sternberg, D. B. Epinephrine-induced learning under anesthesia: Retention performance at several training-testing intervals. Behav. Neurosci. 99, 1019–1022 (1985)

  19. 19

    Ghoneim, M. M. & Block, R. I. Learning and memory during general anesthesia: An update. Anesthesiology 87, 387–410 (1997)

  20. 20

    Weinberger, N. M., Gold, P. E. & Sternberg, D. B. Epinephrine enables Pavlovian fear conditioning under anesthesia. Science 223, 605–607 (1984)

  21. 21

    Sacchetti, B., Lorenzini, C. A., Baldi, E., Tassoni, G. & Bucherelli, C. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J. Neurosci. 19 21, 9570–9578 (1999)

  22. 22

    Rosenkranz, J. A. & Grace, A. A. Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J. Neurosci. 22 (1), 324–337 (2002)

  23. 23

    Andreasen, N. C. et al. Positive and negative symptoms of schizophrenia: past, present, and future. Acta Psychiatrica Scan. (Suppl.) 384, 51–59 (1994)

  24. 24

    Morrison, R. L., Bellack, A. S. & Mueser, K. T. Deficits in facial-affect recognition and schizophrenia. Schiz. Bull. 14 (1), 67–83 (1988)

  25. 25

    Grossberg, S. The imbalanced brain: from normal behaviour to schizophrenia. Biol. Psychiatry 48, 81–98 (2000)

  26. 26

    Nigg, J. T. Is ADHD a disinhibitory disorder? Psychol. Bull. 127, 571–598 (2001)

  27. 27

    McGough, J. J. & McCracken, J. T. Assessment of attention deficit hyperactivity disorder: a review of recent literature. Curr. Opin. Ped. 12, 319–324 (2000)

Download references

Acknowledgements

We thank N. MacMurdo, C. Smolak and B. Lowry for technical assistance, and H. Moore, A. R. West and S. Stocker for discussions. Support was provided by National Institutes of Health grants.

Author information

Correspondence to J. Amiel Rosenkranz.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Further reading

Figure 1: Stimulus-evoked responses in amygdala (LAT) neurons.
Figure 2: Opposing effects of habituation and conditioning on LAT neurons.
Figure 3: Dopamine receptor antagonism blocks enhancement of the odour-evoked response caused by the conditioning procedure.
Figure 4: Neuronal excitability is enhanced by the conditioning procedure, which is blocked by dopamine receptor antagonism.
Figure 5: The pavlovian conditioning procedure reduces spontaneous PSPs via dopamine receptor activation.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.