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The Journal of Neuroscience, May 19, 2004, 24(20):4807-4817; doi:10.1523/JNEUROSCI.5113-03.2004

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Behavioral/Systems/Cognitive
Serotonergic Regulation of Membrane Potential in Developing Rat Prefrontal Cortex: Coordinated Expression of 5-Hydroxytryptamine (5-HT)_1A, 5-HT_2A, and 5-HT₇ Receptors

Jean-Claude Béïque,^1,2 Brian Campbell,¹ Paul Perring,^1,2 Mark W. Hamblin,⁴ Paul Walker,³ Ljiljana Mladenovic,^1,2 and Rodrigo Andrade^1,2

Departments of ¹Psychiatry and Behavioral Neurosciences, ²Pharmacology, and ³Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, Michigan 48201, and ⁴Geriatric Research, Education, and Clinical Center, Veterans Affairs Puget Sound Health Care System, Departments of Psychiatry and Behavioral Sciences, University of Washington, Seattle, Washington 98108

The developing prefrontal cortex receives a dense serotonergic innervation, yet little is known about the actions of serotonin [5-Hydroxytryptamine (5-HT)] in this region during development. Here, we examined the developmental regulation of 5-HT receptors controlling the excitability of pyramidal neurons of this region. Using whole-cell recordings in in vitro brain slices, we identified a dramatic shift in the effects of 5-HT on membrane potential during the postnatal developmental period. In slices derived from young animals [postnatal day (P) 6 to P19], administration of 5-HT elicits a robust depolarization of layer V pyramidal neurons, which gradually shifts to a hyperpolarization commencing during the third postnatal week. This progression is the result of coordinated changes in the function of 5-HT₇ and 5-HT_2A receptors, which mediate different aspects of the depolarization, and of 5-HT_1A receptors, which signal the late developing hyperpolarization. The loss of the 5-HT₇ receptor-mediated depolarization and the appearance of the 5-HT_1A receptor-mediated hyperpolarization appears to reflect changes in receptor expression. In contrast, the decline in the 5-HT_2A receptor depolarization with increasing age was associated with changes in the effectiveness with which these receptors could elicit a membrane depolarization, rather than loss of the receptors per se. Together, these results outline coordinated changes in the serotonergic regulation of cortical excitability at a time of extensive synaptic development and thus suggest a key role for these receptor subtypes in the postnatal development of the prefrontal cortex.

Key words: 5-HT; serotonin; in situ hybridization; postnatal development; prefrontal cortex; in vitro electrophysiology; single-cell RT-PCR

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Received Nov 19, 2003; revised March 29, 2004; accepted March 29, 2004.

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