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The Journal of Neuroscience, November 8, 2006, 26(45):11682-11694; doi:10.1523/JNEUROSCI.3656-06.2006

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Development/Plasticity/Repair
Different Types of Cerebellar GABAergic Interneurons Originate from a Common Pool of Multipotent Progenitor Cells

Ketty Leto,^1 * Barbara Carletti,^1 * Ian Martin Williams,¹ Lorenzo Magrassi,² and Ferdinando Rossi¹

¹Department of Neuroscience and Rita Levi Montalcini Centre for Brain Repair, University of Turin, 10125 Turin, Italy, and ²Neurosurgery, Department of Surgery, Istituto di Ricovero e Cura a Carattere Scientifico Policlinico San Matteo, University of Pavia, 27100 Pavia, Italy

Correspondence should be addressed to Barbara Carletti, Rita Levi Montalcini Center for Brain Repair, Department of Neuroscience, Section of Physiology, University of Turin, Corso Raffaello 30, I-10125 Turin, Italy. Email: barbara.carletti{at}unito.it

Different cerebellar phenotypes are generated according to a precise spatiotemporal schedule, in which projection neurons precede local interneurons. Glutamatergic neurons develop from the rhombic lip, whereas GABAergic neurons originate from the ventricular neuroepithelium. Progenitors in these germinal layers are committed toward specific phenotypes already at early ontogenetic stages. GABAergic interneurons are thought to derive from a subset of ventricular zone cells, which migrate in the white matter and proliferate up to postnatal life. During this period, different interneuron categories are produced according to an inside-out sequence, from the deep nuclei to the molecular layer (we show here that nuclear interneurons are also born during late embryonic and early postnatal days, after glutamatergic and GABAergic projection neurons). To ask whether distinct interneuron phenotypes share common precursors or derive from multiple fate-restricted progenitors, we examined the behavior of embryonic and postnatal rat cerebellar cells heterotopically/heterochronically transplanted to syngenic hosts. In all conditions, donor cells achieved a high degree of integration in the cerebellar cortex and deep nuclei and acquired GABAergic interneuron phenotypes appropriate for the host age and engraftment site. Therefore, contrary to other cerebellar types, which derive from dedicated precursors, GABAergic interneurons are produced by a common pool of progenitors, which maintain their full developmental potentialities up to late ontogenetic stages and adopt mature identities in response to local instructive cues. In this way, the numbers and types of inhibitory interneurons can be set by spatiotemporally patterned signals to match the functional requirements of developing cerebellar circuits.

Key words: cell specification; differentiation; heterotopic/heterochronic transplantation; cerebellar development; neural precursor; inhibitory interneuron

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Received May 11, 2006; accepted Sept. 28, 2006.

Correspondence should be addressed to Barbara Carletti, Rita Levi Montalcini Center for Brain Repair, Department of Neuroscience, Section of Physiology, University of Turin, Corso Raffaello 30, I-10125 Turin, Italy. Email: barbara.carletti{at}unito.it

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