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Preferential targeting of lateral entorhinal inputs onto newly integrated granule cells

View ORCID ProfileNicholas I. Woods, View ORCID ProfileChristopher E. Vaaga, Christina Chatzi, Jaimie D. Adelson, Matthew F. Collie, Julia V. Perederiy, Kenneth R. Tovar, Gary L. Westbrook
doi: https://doi.org/10.1101/153767
Nicholas I. Woods
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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  • ORCID record for Nicholas I. Woods
Christopher E. Vaaga
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Christina Chatzi
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Jaimie D. Adelson
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Matthew F. Collie
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Julia V. Perederiy
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Kenneth R. Tovar
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Gary L. Westbrook
1Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland OR, 97239, USA
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Abstract

Mature dentate granule cells in the hippocampus receive input from the entorhinal cortex via the perforant path in precisely arranged lamina, with medial entorhinal axons innervating the middle molecular layer and lateral entorhinal cortex axons innervating the outer molecular layer. Although vastly outnumbered by mature granule cells, adult-generated newborn granule cells play a unique role in hippocampal function, which has largely been attributed to their enhanced excitability and plasticity (Schmidt-Hieber et al., 2004; Ge et al., 2007). Inputs from the medial and lateral entorhinal cortex carry different informational content, thus the distribution of inputs onto newly integrated granules will affect their function in the circuit. Therefore we examined the functional innervation and synaptic maturation of newly-generated dentate granule cells using retroviral labeling in combination with selective optogenetic activation of medial or lateral entorhinal inputs. Our results indicate that lateral entorhinal inputs provide nearly all the functional innervation of newly integrated granule cells. Despite preferential functional targeting, the dendritic spine density of immature granule cells was not increased in the outer molecular layer compared to the middle molecular layer. However, chronic blockade of neurotransmitter release in medial entorhinal axons with tetanus toxin disrupted normal synapse development from both medial and lateral entorhinal inputs. Our results support a role for preferential lateral perforant path input onto newly generated neurons in mediating pattern separation, but also indicates that medial perforant path input is necessary for normal synaptic development.

Significance Statement The formation of episodic memories involves the integration of contextual and spatial information. Newly integrated neurons in the dentate gyrus of the hippocampus play a critical role in this process, despite constituting only a minor fraction of total granule cells. Here we demonstrate that these neurons preferentially receive information thought to convey the context of an experience - a unique role that each newly integrated granule cell serves for about a month before reaching maturity.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 23, 2017.
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Preferential targeting of lateral entorhinal inputs onto newly integrated granule cells
Nicholas I. Woods, Christopher E. Vaaga, Christina Chatzi, Jaimie D. Adelson, Matthew F. Collie, Julia V. Perederiy, Kenneth R. Tovar, Gary L. Westbrook
bioRxiv 153767; doi: https://doi.org/10.1101/153767
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Preferential targeting of lateral entorhinal inputs onto newly integrated granule cells
Nicholas I. Woods, Christopher E. Vaaga, Christina Chatzi, Jaimie D. Adelson, Matthew F. Collie, Julia V. Perederiy, Kenneth R. Tovar, Gary L. Westbrook
bioRxiv 153767; doi: https://doi.org/10.1101/153767

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