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Edited by Richard L. Huganir, The Johns Hopkins University School of Medicine, Baltimore, MD, and approved August 31, 2012 (received for review April 18, 2012)
Abstract
Although cholinergic innervation of the cortex by the nucleus basalis (NB) is known to modulate cortical neuronal responses and instruct cortical plasticity, little is known about the underlying cellular mechanisms. Using cell-attached recordings in vivo, we demonstrate that electrical stimulation of the NB, paired with visual stimulation, can induce significant potentiation of visual responses in excitatory neurons of the primary visual cortex in mice. We further show with in vivo two-photon calcium imaging, ex vivo calcium imaging, and whole-cell recordings that this pairing-induced potentiation is mediated by direct cholinergic activation of primary visual cortex astrocytes via muscarinic AChRs. The potentiation is absent in conditional inositol 1,4,5 trisphosphate receptor type 2 KO mice, which lack astrocyte calcium activation, and is stimulus-specific, because pairing NB stimulation with a specific visual orientation reveals a highly selective potentiation of responses to the paired orientation compared with unpaired orientations. Collectively, these findings reveal a unique and surprising role for astrocytes in NB-induced stimulus-specific plasticity in the cerebral cortex.
Footnotes
↵1N.C. and H.S. contributed equally to this work.
- ↵2To whom correspondence should be addressed. E-mail: msur{at}mit.edu.
Author contributions: N.C., H.S., and M.S. designed research; N.C., H.S., J.S., G.P., and C.L. performed research; J.P. contributed new reagents/analytic tools; N.C., H.S., and G.P. analyzed data; and N.C. and M.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1206557109/-/DCSupplemental.
Stimulus-specific plasticity is astrocyte-mediated
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