Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy

Nature Neuroscience

Volumn 8, Issue 8, 2005, Pages 1059-1068

  Cobos, Inma ^a   Calcagnotto, Maria Elisa ^b   Vilaythong, Alex J ^c   Thwin, Myo T ^a   Noebels, Jeffrey L ^c   Baraban, Scott C ^b   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALRETININ; PARVALBUMIN; SOMATOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL LOSS; CELL TRANSPLANTATION; CONTROLLED STUDY; DLX1 GENE; ELECTROGRAPHY; EPILEPSY; FOREBRAIN; GENE; GENE MUTATION; HIPPOCAMPUS; HISTOPATHOLOGY; INTERNEURON; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BIPOLAR GANGLION CELL;

AGING; ANIMALS; APOPTOSIS; BEHAVIOR, ANIMAL; BRAIN; CELL COUNT; CEREBRAL CORTEX; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GENE DELETION; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 23044437148     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1499     Document Type: Article

References (49)

1. Noebels, J.L. The biology of epilepsy genes. Annu. Rev. Neurosci. 26, 599-625 (2003).
2. Paulsen, O. & Moser, E.I. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21, 273-278 (1998).
3. Whittington, M.A. & Traub, R.D. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 26, 676-682 (2003).
4. Freund, T.F. Interneuron Diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci. 26, 489-495 (2003).
5. Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807 (2004).
6. Ramon y Cajal, S. Histology of the Nervous System. (Oxford University Press, New York, 1911).
7. Jones, E.G. Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. Comp. Neurol. 160, 205-267 (1975).
8. DeFelipe, J. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb. Cortex 3, 273-289 (1993).
9. Kubota, Y., Hattori, R. & Yui, Y. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649, 159-173 (1994).
10. Gonchar, Y. & Burkhalter, A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347-358 (1997).
11. McBain, C.J. & Fisahn, A. Interneurons unbound. Nat. Rev. Neurosci. 2, 11-23 (2001).
12. Gupta, A., Wang, Y. & Markram, H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273-278 (2000).
13. Klausberger, T. et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848 (2003).
14. Lavdas, A.A., Grigoriou, M., Pachnis, V. & Parnavelas, J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888 (1999).
15. Sussel, L., Marin, O., Kimura, S. & Rubenstein, J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359-3370 (1999).
16. Wichterle, H., Garcia-Verdugo, J.M., Herrera, D.G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461-466 (1999).
17. Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J.L. & Anderson, S.A. Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622 (2004).
18. Marin, O., Anderson, S.A. & Rubenstein, J.L. Origin and molecular specification of striatal interneurons. J. Neurosci. 20, 6063-6076 (2000).
19. Letinic, K., Zoncu, R. & Rakic, P. Origin of GABAergic neurons in the human neocortex. Nature 417, 645-649 (2002).
20. Panganiban, G. & Rubenstein, J.L. Developmental functions of the Distal-less/Dlx homeobox genes. Development 129, 4371-4386 (2002).
21. Qiu, M. et al. Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev. 9, 2523-2538 (1995).
22. Qiu, M. et al. Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev. Biol. 185, 165-184 (1997).
23. Anderson, S.A., Eisenstat, D.D., Shi, L. & Rubenstein, J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476 (1997).
24. Cobos, I., Broccoli, V. & Rubenstein, J.L. The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain. J. Comp. Neurol. 483, 292-303 (2005).
25. Kitamura, K. et al. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat. Genet. 32, 359-369 (2002).
26. Marty, S., Berzaghi Mda, P. & Berninger, B. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci. 20, 198-202 (1997).
27. Stuhmer, T., Puelles, L., Ekker, M. & Rubenstein, J.L. Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb. Cortex 12, 75-85 (2002).
28. Saino-Saito, S., Berlin, R. & Baker, H. Dlx-1 and Dlx-2 expression in the adult mouse brain: relationship to dopaminergic phenotypic regulation. J. Comp. Neurol. 461, 18-30 (2003).
29. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486 (1997).
30. Alifragis, P., Liapi, A. & Parnavelas, J.G. Lhx6 regulates the migration of cortical interneurons from the ventral telencephalon but does not specify their GABA phenotype. J. Neurosci. 24, 5643-5648 (2004).
31. Alcantara, S. et al. Regional and cellular patterns of Reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18, 7779-7799 (1998).
32. Erbel-Sieler, C. et al. Behavioral and regulatory abnormalities in mice deficient in the NPAS1 and NPAS3 transcription factors. Proc. Natl. Acad. Sci. USA 101, 13648-13653 (2004).
33. Stuhmer, T., Anderson, S.A., Ekker, M. & Rubenstein, J.L. Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129, 245-252 (2002).
34. McBain, C.J., Eaton, J.V., Brown, T. & Dingledine, R. CNQX increases spontaneous inhibitory input to CA3 pyramidal neurones in neonatal rat hippocampal slices. Brain Res. 592, 255-260 (1992).
35. Morimoto, K., Fahnestock, M. & Racine, R.J. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog. Neurobiol. 73, 1-60 (2004).
36. Baraban, S.C. & Tallent, M.K. Interneuron Diversity series: Interneuronal neuropeptides-endogenous regulators of neuronal excitability. Trends Neurosci. 27, 135-142 (2004).
37. Racine, R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294 (1972).
38. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325-340 (2002).
39. Nery, S., Fishell, G. & Corbin, J.G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5, 1279-1287 (2002).
40. Yun, K. et al. Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129, 5029-5040 (2002).
41. Powell, E.M. et al. Genetic disruption of cortical interneuron development causes region-and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J. Neurosci. 23, 622-631 (2003).
42. Kobayashi, M. & Buckmaster, P.S. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J. Neurosci. 23, 2440-2452 (2003).
43. Cossart, R. et al. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4, 52-62 (2001).
44. Cossart, R., Bernard, C. & Ben-Ari, Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci. 28, 108-115 (2005).
45. Maccaferri, G., Roberts, J.D., Szucs, P., Cottingham, C.A. & Somogyi, P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. (Lond.) 524, 91-116 (2000).
46. Gonchar, Y., Turney, S., Price, J.L. & Burkhalter, A. Axo-axonic synapses formed by somatostatin-expressing GABAergic neurons in rat and monkey visual cortex. J. Comp. Neurol. 443, 1-14 (2002).
47. Wang, Y. et al. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. (Lond.) 561, 65-90 (2004).
48. Levitt, P., Eagleson, K.L. & Powell, E.M. Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci. 27, 400-406 (2004).
49. Horike, S., Cai, S., Miyano, M., Cheng, J.F. & Kohwi-Shigematsu, T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet. 37, 31-40 (2005).