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The Journal of Neuroscience, April 4, 2007, 27(14):3813-3822; doi:10.1523/JNEUROSCI.5124-06.2007

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Development/Plasticity/Repair
Dopamine Receptor Activation Modulates GABA Neuron Migration from the Basal Forebrain to the Cerebral Cortex

James E. Crandall,¹ Deirdre M. McCarthy,² Kiyomi Y. Araki,² John R. Sims,^2,3 Jia-Qian Ren,³ and Pradeep G. Bhide²

¹Eunice Kennedy Shriver Center for Mental Retardation, Physiology, University of Massachusetts Medical School, Waltham, Massachusetts 02452, and Departments of ²Neurology and ³Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02129

Correspondence should be addressed to Dr. Pradeep G. Bhide, Developmental Neurobiology, Massachusetts General Hospital, 149 13th Street, Charlestown, MA 02129. Email: bhide{at}helix.mgh.harvard.edu

GABA neurons of the cerebral cortex and other telencephalic structures are produced in the basal forebrain and migrate to their final destinations during the embryonic period. The embryonic basal forebrain is enriched in dopamine and its receptors, creating a favorable environment for dopamine to influence GABA neuron migration. However, whether dopamine receptor activation can influence GABA neuron migration is not known. We show that dopamine D₁ receptor activation promotes and D₂ receptor activation decreases GABA neuron migration from the medial and caudal ganglionic eminences to the cerebral cortex in slice preparations of embryonic mouse forebrain. Slice preparations from D₁ or D₂ receptor knock-out mouse embryos confirm the findings. In addition, D₁ receptor electroporation into cells of the basal forebrain and pharmacological activation of the receptor promote migration of the electroporated cells to the cerebral cortex. Analysis of GABA neuron numbers in the cerebral wall of the dopamine receptor knock-out mouse embryos further confirmed the effects of dopamine receptor activation on GABA neuron migration. Finally, dopamine receptor activation mobilizes striatal neuronal cytoskeleton in a manner consistent with the effects on neuronal migration. These data show that impairing the physiological balance between D₁ and D₂ receptors can alter GABA neuron migration from the basal forebrain to the cerebral cortex. The intimate relationship between dopamine and GABA neuron development revealed here may offer novel insights into developmental disorders such as schizophrenia, attention deficit or autism, and fetal cocaine exposure, all of which are associated with dopamine and GABA imbalance.

Key words: striatum; basal ganglia; ganglionic eminence; dopamine D₁ receptor; dopamine D₂ receptor; tangential neuronal migration

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Received Nov. 27, 2006; revised March 2, 2007; accepted March 6, 2007.

Correspondence should be addressed to Dr. Pradeep G. Bhide, Developmental Neurobiology, Massachusetts General Hospital, 149 13th Street, Charlestown, MA 02129. Email: bhide{at}helix.mgh.harvard.edu

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