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The Journal of Neuroscience, August 12, 2009, 29(32):10094-10103; doi:10.1523/JNEUROSCI.1960-09.2009

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Behavioral/Systems/Cognitive
Layer II/III of the Prefrontal Cortex: Inhibition by the Serotonin 5-HT_1A Receptor in Development and Stress

Nathalie M. Goodfellow,¹ Madhurima Benekareddy,³ Vidita A. Vaidya,³ and Evelyn K. Lambe^1,2

¹Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A8, Canada, ²Department of Obstetrics and Gynaecology, University of Toronto, Toronto, Ontario M5G 1L4, Canada, and ³Department of Biological Sciences, Tata Institute of Fundamental Research, Mumbai 400 005, India

Correspondence should be addressed to Dr. Evelyn K. Lambe, Department of Physiology, University of Toronto, 1 King's College Circle, Toronto, ON M5S 1A8, Canada. Email: evelyn.lambe{at}utoronto.ca

The modulation of the prefrontal cortex by the neurotransmitter serotonin (5-HT) is thought to play a key role in determining adult anxiety levels. Layer II/III of the prefrontal cortex, which mediates communication across cortical regions, displays a high level of 5-HT_1A receptor binding in normal individuals and a significantly lower level in patients with mood and anxiety disorders. Here, we examine how serotonin modulates pyramidal neurons in layer II/III of the rat prefrontal cortex throughout postnatal development and in adulthood. Using whole cell recordings in brain slices of the rat medial prefrontal cortex, we observed that serotonin directly inhibits layer II/III pyramidal neurons through 5-HT_1A receptors across postnatal development (postnatal days 6–96). In adulthood, a sex difference in these currents emerges, consistent with human imaging studies of 5-HT_1A receptor binding. We examined the effects of early life stress on the 5-HT_1A receptor currents in layer II/III. Surprisingly, animals subjected to early life stress displayed significantly larger 5-HT_1A-mediated outward currents throughout the third and fourth postnatal weeks after elevated 5-HT_1A expression during the second postnatal week. Subsequent exposure to social isolation in adulthood resulted in the almost-complete elimination of 5-HT_1A currents in layer II/III neurons suggesting an interaction between early life events and adult experiences. These data represent the first examination of functional 5-HT_1A receptors in layer II/III of the prefrontal cortex during normal development as well as after stress.

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Received April 24, 2009; revised July 8, 2009; accepted July 9, 2009.

Correspondence should be addressed to Dr. Evelyn K. Lambe, Department of Physiology, University of Toronto, 1 King's College Circle, Toronto, ON M5S 1A8, Canada. Email: evelyn.lambe{at}utoronto.ca

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