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The Journal of Neuroscience, June 24, 2009, 29(25):8198-8205; doi:10.1523/JNEUROSCI.0336-09.2009

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Cellular/Molecular
Subcellular Dynamics of Somatostatin Receptor Subtype 1 in the Rat Arcuate Nucleus: Receptor Localization and Synaptic Connectivity Vary in Parallel with the Ultradian Rhythm of Growth Hormone Secretion

Thomas Stroh,^1,2 Martine R. van Schouwenburg,^1,2 Alain Beaudet,^1,2 and Gloria S. Tannenbaum^1,2,3,4

¹Department of Neurology and Neurosurgery and ²Montreal Neurological Institute, McGill University, Montréal, Québec H3A 2B4, Canada, ³Department of Pediatrics, McGill University, Montréal, Québec H3H 1P3, Canada, and ⁴Montreal Children's Hospital Research Institute, Montréal, Québec H3H 1P3, Canada

Correspondence should be addressed to Dr. Thomas Stroh, Montreal Neurological Institute, McGill University, 3801 University Street, Montréal, QC H3A 2B4, Canada. Email: thomas.stroh{at}mcgill.ca

Growth hormone (GH) secretion in male rats exhibits a 3.3 h ultradian rhythm generated by the reciprocal interaction of GH-releasing hormone (GHRH) and somatostatin (SRIF). SRIF receptor subtypes sst₁ and sst₂ are highly expressed in GHRH neurons of the hypothalamic arcuate nucleus (ARC). We previously demonstrated an ultradian oscillation in binding of SRIF analogs to the ARC in relation to GH peaks and troughs. Here we tested the hypothesis that these ultradian changes in SRIF binding are due to differential plasma membrane targeting of sst₁ receptors in ARC neurons using immunocytochemistry and electron microscopy. We found that 87% of sst₁-positive ARC neurons also synthesized GHRH. Subcellularly, 80% of sst₁ receptors were located intracellularly and 20% at the plasma membrane regardless of GH status. However, whereas 30% of the cell-surface sst₁ receptors were located perisynaptically or subsynaptically following exposure to high GH secretion, this fraction was increased to 42% following a GH trough period (p = 0.05). Furthermore, the relative abundance of symmetric and asymmetric synapses on sst₁-positive dendrites also varied significantly, depending on the GH cycle, from approximately equal numbers following GH troughs to 70:30 in favor of symmetric, i.e., inhibitory, inputs after GH peaks (p < 0.02). These findings suggest that postsynaptic localization of sst₁ receptors and synaptic connectivity in the ARC undergo pronounced remodeling in parallel with the GH rhythm. Such synaptic plasticity may be an important mechanism by which sst₁ mediates SRIF's cyclical effects on ARC GHRH neurons to generate the ultradian rhythm of GH secretion.

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Received Jan. 20, 2009; revised April 23, 2009; accepted May 19, 2009.

Correspondence should be addressed to Dr. Thomas Stroh, Montreal Neurological Institute, McGill University, 3801 University Street, Montréal, QC H3A 2B4, Canada. Email: thomas.stroh{at}mcgill.ca

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