Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals

Matthew Ennis, Fuming Zhou, Kelly J. Ciombor, Vassiliki Aroniadou-Anderjaska, Abdallah Hayar, Emiliana Borrelli, Lee A. Zimmer, Frank Margolis, Michael T. Shipley

Research output: Contribution to journalArticle

162 Citations (Scopus)

Abstract

Olfactory receptor neurons of the nasal epithelium project via the olfactory nerve (ON) to the glomeruli of the main olfactory bulb, where they form glutamatergic synapses with the apical dendrites of mitral and tufted cells, the output cells of the olfactory bulb, and with juxtaglomerular interneurons. The glomerular layer contains one of the largest population of dopamine (DA) neurons in the brain, and DA in the olfactory bulb is found exclusively in juxtaglomerular neurons. D2 receptors, the predominant DA receptor subtype in the olfactory bulb, are found in the ON and glomerular layers, and are present on ON terminals. In the present study, field potential and single-unit recordings, as well as whole cell patch-clamp techniques, were used to investigate the role of DA and D2 receptors in glomerular synaptic processing in rat and mouse olfactory bulb slices. DA and D2 receptor agonists reduced ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells. Spontaneous and ON-evoked spiking of mitral cells was also reduced by DA and D2 agonists, and enhanced by D2 antagonists. DA did not produce measurable postsynaptic changes in juxtaglomerular cells, nor did it alter their responses to mitral/tufted cell inputs. DA also reduced 1) paired-pulse depression of ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells and 2) the amplitude and frequency of spontaneous, but not miniature, excitatory postsynaptic currents in juxtaglomerular cells. Taken together, these findings are consistent with the hypothesis that activation of D2 receptors presynaptically inhibits ON terminals. DA and D2 agonists had no effect in D2 receptor knockout mice, suggesting that D2 receptors are the only type of DA receptors that affect signal transmission from the ON to the rodent olfactory bulb.

Original languageEnglish (US)
Pages (from-to)2986-2997
Number of pages12
JournalJournal of Neurophysiology
Volume86
Issue number6
StatePublished - Dec 27 2001
Externally publishedYes

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Olfactory Nerve
Dopamine D2 Receptors
Olfactory Bulb
Dopamine Agonists
Dopamine
Dopamine Receptors
Olfactory Receptor Neurons
Nasal Mucosa
Excitatory Postsynaptic Potentials
Dopaminergic Neurons
Patch-Clamp Techniques
Interneurons
Dendrites
Knockout Mice
Synapses
Rodentia
Neurons

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

Ennis, M., Zhou, F., Ciombor, K. J., Aroniadou-Anderjaska, V., Hayar, A., Borrelli, E., ... Shipley, M. T. (2001). Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. Journal of Neurophysiology, 86(6), 2986-2997.

Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. / Ennis, Matthew; Zhou, Fuming; Ciombor, Kelly J.; Aroniadou-Anderjaska, Vassiliki; Hayar, Abdallah; Borrelli, Emiliana; Zimmer, Lee A.; Margolis, Frank; Shipley, Michael T.

In: Journal of Neurophysiology, Vol. 86, No. 6, 27.12.2001, p. 2986-2997.

Research output: Contribution to journalArticle

Ennis, M, Zhou, F, Ciombor, KJ, Aroniadou-Anderjaska, V, Hayar, A, Borrelli, E, Zimmer, LA, Margolis, F & Shipley, MT 2001, 'Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals', Journal of Neurophysiology, vol. 86, no. 6, pp. 2986-2997.
Ennis M, Zhou F, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E et al. Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. Journal of Neurophysiology. 2001 Dec 27;86(6):2986-2997.
Ennis, Matthew ; Zhou, Fuming ; Ciombor, Kelly J. ; Aroniadou-Anderjaska, Vassiliki ; Hayar, Abdallah ; Borrelli, Emiliana ; Zimmer, Lee A. ; Margolis, Frank ; Shipley, Michael T. / Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. In: Journal of Neurophysiology. 2001 ; Vol. 86, No. 6. pp. 2986-2997.
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