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ARTICLE, Behavioral/Systems

Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission

István Katona, Ede A. Rancz, László Acsády, Catherine Ledent, Ken Mackie, Norbert Hájos and Tamás F. Freund
Journal of Neuroscience 1 December 2001, 21 (23) 9506-9518; DOI: https://doi.org/10.1523/JNEUROSCI.21-23-09506.2001
István Katona
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary,
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Ede A. Rancz
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary,
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László Acsády
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary,
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Catherine Ledent
2Institut de Recherche Interdisciplinaire en Biologie Humaine et Nucléaire, Université libre de Bruxelles, B-1070 Brussels, Belgium, and
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Ken Mackie
3Departments of Anesthesiology, and Physiology and Biophysics, University of Washington, Seattle, Washington 98195
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Norbert Hájos
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary,
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Tamás F. Freund
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary,
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Abstract

Cannabinoids are the most popular illicit drugs used for recreational purposes worldwide. However, the neurobiological substrate of their mood-altering capacity has not been elucidated so far. Here we report that CB1 cannabinoid receptors are expressed at high levels in certain amygdala nuclei, especially in the lateral and basal nuclei, but are absent in other nuclei (e.g., in the central nucleus and in the medial nucleus). Expression of the CB1 protein was restricted to a distinct subpopulation of GABAergic interneurons corresponding to large cholecystokinin-positive cells. Detailed electron microscopic investigation revealed that CB1 receptors are located presynaptically on cholecystokinin-positive axon terminals, which establish symmetrical GABAergic synapses with their postsynaptic targets. The physiological consequence of this particular anatomical localization was investigated by whole-cell patch-clamp recordings in principal cells of the lateral and basal nuclei. CB1 receptor agonists WIN 55,212–2 and CP 55,940 reduced the amplitude of GABAA receptor-mediated evoked and spontaneous IPSCs, whereas the action potential-independent miniature IPSCs were not significantly affected. In contrast, CB1 receptor agonists were ineffective in changing the amplitude of IPSCs in the rat central nucleus and in the basal nucleus of CB1 knock-out mice. These results suggest that cannabinoids target specific elements in neuronal networks of given amygdala nuclei, where they presynaptically modulate GABAergic synaptic transmission. We propose that these anatomical and physiological features, characteristic of CB1 receptors in several forebrain regions, represent the neuronal substrate for endocannabinoids involved in retrograde synaptic signaling and may explain some of the emotionally relevant behavioral effects of cannabinoid exposure.

  • endocannabinoids
  • interneurons
  • inhibition
  • CCK
  • retrograde signaling
  • anxiety
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The Journal of Neuroscience: 21 (23)
Journal of Neuroscience
Vol. 21, Issue 23
1 Dec 2001
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Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission
István Katona, Ede A. Rancz, László Acsády, Catherine Ledent, Ken Mackie, Norbert Hájos, Tamás F. Freund
Journal of Neuroscience 1 December 2001, 21 (23) 9506-9518; DOI: 10.1523/JNEUROSCI.21-23-09506.2001

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Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission
István Katona, Ede A. Rancz, László Acsády, Catherine Ledent, Ken Mackie, Norbert Hájos, Tamás F. Freund
Journal of Neuroscience 1 December 2001, 21 (23) 9506-9518; DOI: 10.1523/JNEUROSCI.21-23-09506.2001
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Keywords

  • endocannabinoids
  • interneurons
  • inhibition
  • CCK
  • retrograde signaling
  • anxiety

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