A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity

Matteo Bergami; Giacomo  Masserdotti; Silvio G Temprana; Elisa Motori; Therese M Eriksson; Jana Göbel; Sun Min Yang; Karl-Klaus Conzelmann; Alejandro F  Schinder; Magdalena Götz; Benedikt Berninger

doi:10.1016/j.neuron.2015.01.001

A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity

Matteo Bergami, Giacomo Masserdotti, Silvio G Temprana, Elisa Motori, Therese M Eriksson, Jana Göbel, Sun Min Yang, Karl-Klaus Conzelmann, Alejandro F Schinder, Magdalena Götz, Benedikt Berninger

Developmental Neurobiology

Research output: Contribution to journal › Article › peer-review

154 Citations (Scopus)

Abstract

Neurogenesis in the dentate gyrus (DG) of the adult hippocampus is a process regulated by experience. To understand whether experience also modifies the connectivity of new neurons, we systematically investigated changes in their innervation following environmental enrichment (EE). We found that EE exposure between 2–6 weeks following neuron birth, rather than merely increasing the number of new neurons, profoundly affected their pattern of monosynaptic inputs. Both local innervation by interneurons and to even greater degree long-distance innervation by cortical neurons were markedly enhanced. Furthermore, following EE, new neurons received inputs from CA3 and CA1 inhibitory neurons that were rarely observed under control conditions. While EE-induced changes in inhibitory innervation were largely transient, cortical innervation remained increased after returning animals to control conditions. Our findings demonstrate an unprecedented experience-dependent reorganization of connections impinging onto adult-born neurons, which is likely to have important impact on their contribution to hippocampal information processing.

Original language	English
Pages (from-to)	710-717
Journal	Neuron
Volume	85
Issue number	4
Early online date	5 Feb 2015
DOIs	https://doi.org/10.1016/j.neuron.2015.01.001
Publication status	Published - 18 Feb 2015

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title = "A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity",

abstract = "Neurogenesis in the dentate gyrus (DG) of the adult hippocampus is a process regulated by experience. To understand whether experience also modifies the connectivity of new neurons, we systematically investigated changes in their innervation following environmental enrichment (EE). We found that EE exposure between 2–6 weeks following neuron birth, rather than merely increasing the number of new neurons, profoundly affected their pattern of monosynaptic inputs. Both local innervation by interneurons and to even greater degree long-distance innervation by cortical neurons were markedly enhanced. Furthermore, following EE, new neurons received inputs from CA3 and CA1 inhibitory neurons that were rarely observed under control conditions. While EE-induced changes in inhibitory innervation were largely transient, cortical innervation remained increased after returning animals to control conditions. Our findings demonstrate an unprecedented experience-dependent reorganization of connections impinging onto adult-born neurons, which is likely to have important impact on their contribution to hippocampal information processing.",

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AU - Bergami, Matteo

AU - Masserdotti, Giacomo

AU - Temprana, Silvio G

AU - Motori, Elisa

AU - Eriksson, Therese M

AU - Göbel, Jana

AU - Yang, Sun Min

AU - Conzelmann, Karl-Klaus

AU - Schinder, Alejandro F

AU - Götz, Magdalena

AU - Berninger, Benedikt

PY - 2015/2/18

Y1 - 2015/2/18

N2 - Neurogenesis in the dentate gyrus (DG) of the adult hippocampus is a process regulated by experience. To understand whether experience also modifies the connectivity of new neurons, we systematically investigated changes in their innervation following environmental enrichment (EE). We found that EE exposure between 2–6 weeks following neuron birth, rather than merely increasing the number of new neurons, profoundly affected their pattern of monosynaptic inputs. Both local innervation by interneurons and to even greater degree long-distance innervation by cortical neurons were markedly enhanced. Furthermore, following EE, new neurons received inputs from CA3 and CA1 inhibitory neurons that were rarely observed under control conditions. While EE-induced changes in inhibitory innervation were largely transient, cortical innervation remained increased after returning animals to control conditions. Our findings demonstrate an unprecedented experience-dependent reorganization of connections impinging onto adult-born neurons, which is likely to have important impact on their contribution to hippocampal information processing.

AB - Neurogenesis in the dentate gyrus (DG) of the adult hippocampus is a process regulated by experience. To understand whether experience also modifies the connectivity of new neurons, we systematically investigated changes in their innervation following environmental enrichment (EE). We found that EE exposure between 2–6 weeks following neuron birth, rather than merely increasing the number of new neurons, profoundly affected their pattern of monosynaptic inputs. Both local innervation by interneurons and to even greater degree long-distance innervation by cortical neurons were markedly enhanced. Furthermore, following EE, new neurons received inputs from CA3 and CA1 inhibitory neurons that were rarely observed under control conditions. While EE-induced changes in inhibitory innervation were largely transient, cortical innervation remained increased after returning animals to control conditions. Our findings demonstrate an unprecedented experience-dependent reorganization of connections impinging onto adult-born neurons, which is likely to have important impact on their contribution to hippocampal information processing.

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JO - Neuron

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A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity

Abstract

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