Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb

Kurt A. Sailor, Matthew T. Valley, Martin T. Wiechert, Hermann Riecke, Gerald J. Sun, Wayne Adams, James C. Dennis, Shirin Sharafi, Guo li Ming, Hongjun Song, Pierre Marie Lledo

Research output: Contribution to journalArticle

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. Using in vivo imaging, Sailor and Valley et al. (2016) show matching, robust structural plasticity in olfactory bulb granule and mitral/tufted cell synapses. Computational modeling shows this structural plasticity is compatible with stable memory and high adaptability to changing sensory inputs.

Original languageEnglish (US)
JournalNeuron
DOIs
StateAccepted/In press - Oct 15 2015

Fingerprint

Olfactory Bulb
Automatic Data Processing
Interneurons
Neuronal Plasticity
Synapses
Neurons
Dendritic Spines
Computer Simulation
Learning
Brain

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Sailor, K. A., Valley, M. T., Wiechert, M. T., Riecke, H., Sun, G. J., Adams, W., ... Lledo, P. M. (Accepted/In press). Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb. Neuron. https://doi.org/10.1016/j.neuron.2016.06.004

Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb. / Sailor, Kurt A.; Valley, Matthew T.; Wiechert, Martin T.; Riecke, Hermann; Sun, Gerald J.; Adams, Wayne; Dennis, James C.; Sharafi, Shirin; Ming, Guo li; Song, Hongjun; Lledo, Pierre Marie.

In: Neuron, 15.10.2015.

Research output: Contribution to journalArticle

Sailor, KA, Valley, MT, Wiechert, MT, Riecke, H, Sun, GJ, Adams, W, Dennis, JC, Sharafi, S, Ming, GL, Song, H & Lledo, PM 2015, 'Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb', Neuron. https://doi.org/10.1016/j.neuron.2016.06.004
Sailor, Kurt A. ; Valley, Matthew T. ; Wiechert, Martin T. ; Riecke, Hermann ; Sun, Gerald J. ; Adams, Wayne ; Dennis, James C. ; Sharafi, Shirin ; Ming, Guo li ; Song, Hongjun ; Lledo, Pierre Marie. / Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb. In: Neuron. 2015.
@article{94fe4b30ac4c425db17e455369219fd8,
title = "Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb",
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. Using in vivo imaging, Sailor and Valley et al. (2016) show matching, robust structural plasticity in olfactory bulb granule and mitral/tufted cell synapses. Computational modeling shows this structural plasticity is compatible with stable memory and high adaptability to changing sensory inputs.",
author = "Sailor, {Kurt A.} and Valley, {Matthew T.} and Wiechert, {Martin T.} and Hermann Riecke and Sun, {Gerald J.} and Wayne Adams and Dennis, {James C.} and Shirin Sharafi and Ming, {Guo li} and Hongjun Song and Lledo, {Pierre Marie}",
year = "2015",
month = "10",
day = "15",
doi = "10.1016/j.neuron.2016.06.004",
language = "English (US)",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",

}

TY - JOUR

T1 - Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb

AU - Sailor, Kurt A.

AU - Valley, Matthew T.

AU - Wiechert, Martin T.

AU - Riecke, Hermann

AU - Sun, Gerald J.

AU - Adams, Wayne

AU - Dennis, James C.

AU - Sharafi, Shirin

AU - Ming, Guo li

AU - Song, Hongjun

AU - Lledo, Pierre Marie

PY - 2015/10/15

Y1 - 2015/10/15

N2 - 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. Using in vivo imaging, Sailor and Valley et al. (2016) show matching, robust structural plasticity in olfactory bulb granule and mitral/tufted cell synapses. Computational modeling shows this structural plasticity is compatible with stable memory and high adaptability to changing sensory inputs.

AB - 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. Using in vivo imaging, Sailor and Valley et al. (2016) show matching, robust structural plasticity in olfactory bulb granule and mitral/tufted cell synapses. Computational modeling shows this structural plasticity is compatible with stable memory and high adaptability to changing sensory inputs.

UR - http://www.scopus.com/inward/record.url?scp=84978520155&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84978520155&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2016.06.004

DO - 10.1016/j.neuron.2016.06.004

M3 - Article

C2 - 27373833

AN - SCOPUS:84978520155

JO - Neuron

JF - Neuron

SN - 0896-6273

ER -