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Rothwell, Patrick E.; Fuccillo, Marc V.; Maxeiner, Stephan; Hayton, Scott J.; Gokce, Ozgun; Lim, Byung Kook; Fowler, Stephen C.; Malenka, Robert C.; Südhof, Thomas C.
Cell, 07/2014, Volume: 158, Issue: 1Journal Article
In humans, neuroligin-3 mutations are associated with autism, whereas in mice, the corresponding mutations produce robust synaptic and behavioral changes. However, different neuroligin-3 mutations cause largely distinct phenotypes in mice, and no causal relationship links a specific synaptic dysfunction to a behavioral change. Using rotarod motor learning as a proxy for acquired repetitive behaviors in mice, we found that different neuroligin-3 mutations uniformly enhanced formation of repetitive motor routines. Surprisingly, neuroligin-3 mutations caused this phenotype not via changes in the cerebellum or dorsal striatum but via a selective synaptic impairment in the nucleus accumbens/ventral striatum. Here, neuroligin-3 mutations increased rotarod learning by specifically impeding synaptic inhibition onto D1-dopamine receptor-expressing but not D2-dopamine receptor-expressing medium spiny neurons. Our data thus suggest that different autism-associated neuroligin-3 mutations cause a common increase in acquired repetitive behaviors by impairing a specific striatal synapse and thereby provide a plausible circuit substrate for autism pathophysiology. Display omitted Display omitted •Neuroligin-3 mutations commonly enhance repetitive motor routines in mice•Repetitive behavior requires neuroligin-3 function in the nucleus accumbens•Neuroligin-3 is selectively essential in D1-dopamine receptor-containing neurons•Neuroligin-3 deletion impairs synaptic inhibition on striatal medium spiny neurons Different neuroligin-3 mutations cause a common enhancement of repetitive behaviors by a selective effect in one particular type of medium spiny neuron in one particular brain region, the nucleus accumbens of the ventral striatum, in mice.
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