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Edited* by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved October 9, 2014 (received for review January 24, 2014)
Significance
Proper recruitment of inhibitory interneurons is crucial to configuring cortical neural circuits for information processing and propagation, but the development of synaptic inputs to these interneurons is not well-understood. We traced the sources of long-range and local inputs to a major interneuron subtype, the parvalbumin-positive interneurons (PVNs), in mouse visual cortex. Whereas the long-range inputs show strong short-term synaptic depression, local recurrent inputs gradually lose such depression during postnatal maturation. We further uncovered the circuitry and molecular mechanisms that contribute to this source-dependent maturation in synaptic inputs. Although short-term depression of long-range inputs is well-suited for afferent signal detection, the robust synaptic dynamics of local inputs may facilitate rapid and proportional PVN recruitment for regulating network operations.
Abstract
Cortical networks consist of local recurrent circuits and long-range pathways from other brain areas. Parvalbumin-positive interneurons (PVNs) regulate the dynamic operation of local ensembles as well as the temporal precision of afferent signals. The synaptic recruitment of PVNs that support these circuit operations is not well-understood. Here we demonstrate that the synaptic dynamics of PVN recruitment in mouse visual cortex are customized according to input source with distinct maturation profiles. Whereas the long-range inputs to PVNs show strong short-term depression throughout postnatal maturation, local inputs from nearby pyramidal neurons progressively lose such depression. This enhanced local recruitment depends on PVN-mediated reciprocal inhibition and results from both pre- and postsynaptic mechanisms, including calcium-permeable AMPA receptors at PVN postsynaptic sites. Although short-term depression of long-range inputs is well-suited for afferent signal detection, the robust dynamics of local inputs may facilitate rapid and proportional PVN recruitment in regulating local circuit operations.
Footnotes
- ↵1To whom correspondence should be addressed. Email: huangj{at}cshl.edu.
Author contributions: J.L. and Z.J.H. designed research; J.L. and J.T. performed research; Y.L. contributed new reagents/analytic tools; J.L. and J.T. analyzed data; and J.L. and Z.J.H. wrote the paper.
The authors declare no conflict of interest.
↵*This Direct Submission article had a prearranged editor.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1400694111/-/DCSupplemental.
Synapse-specific maturation of PV neurons
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