Abstract
In the mammalian brain, the anatomical structure of neural circuits changes little during adulthood. As a result, adult learning and memory are thought to result from specific changes in synaptic strength. A possible exception is the olfactory bulb (OB), where activity guides interneuron turnover throughout adulthood. These adult-born granule cell (GC) interneurons form new GABAergic synapses that have little synaptic strength plasticity. In the face of persistent neuronal and synaptic turnover, how does the OB balance flexibility, as is required for adapting to changing sensory environments, with perceptual stability? Here we show that high dendritic spine turnover is a universal feature of GCs, regardless of their developmental origin and age. We find matching dynamics among postsynaptic sites on the principal neurons receiving the new synaptic inputs. We further demonstrate in silico that this coordinated structural plasticity is consistent with stable, yet flexible, decorrelated sensory representations. Together, our study reveals that persistent, coordinated synaptic structural plasticity between interneurons and principal neurons is a major mode of functional plasticity in the OB.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 384-396 |
| Number of pages | 13 |
| Journal | Neuron |
| Volume | 91 |
| Issue number | 2 |
| DOIs | |
| State | Published - Jul 20 2016 |
Funding
We thank Eileen Huang for data analysis; Soham Saha, Camille Mazo, Gabriel Lepousez, and Cyrille Norotte for manual puncta analysis; Dwight Bergels, David Linden, Randall Reed, Richard Huganir, and Chun Zhong for advice; Anne Lanjuin for providing Tbet-Cre mice; Elly Nedivi and Jerry Chen for providing the gephyrin-teal construct; and David DiGregorio for managing the Pasteur Institute Shared Neuroscience Department imaging facility funded by “Ile de France Domaine d’Intérêt Majeur (NeRF).” HPC Northwestern University provided HPC access (Quest). Support was provided by the following: W.A. and J.C.D., NSF undergraduate support RTG DMS-0636574; K.A.S., P.M.L., M.T.V., and M.T.W., “AG2R-La-Mondiale” life insurance, Agence Nationale de la Recherche ANR-15-CE37-0004-01, NIH US-French Research Proposal Grants #1R01DC015137-01 and ANR-15-NEUC-0004 (Circuit-OPL), the Laboratory for Excellence “Revive” Program (Investissement d’Avenir, ANR-10-LABX-73) and “Biopsy” (Investissement d’Avenir, ANR-11-IDEX-0004-02); K.A.S., NIH NRSA F31NS066612 and “Revive” fellowships; M.T.V., Pasteur-Roux fellowship and the Phillippe Foundation. H.J.S., NIH R37NS047344; G.L.M., NIH R01MH105128 and NIH R01NS048271, and the authors acknowledge the joint participation by the Diana Helis Henry Medical Research Foundation through its direct engagement in the continuous active conduct of medical research in conjunction with The Johns Hopkins Hospital and the Johns Hopkins University School of Medicine and the Foundation’s Parkinson’s Disease Program (No. H-1).
ASJC Scopus subject areas
- General Neuroscience