Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse

The long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactio...

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Main Authors: Joachim Ahlbeck, Lingzhen Song, Mattia Chini, Sebastian H Bitzenhofer, Ileana L Hanganu-Opatz
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/33158
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author Joachim Ahlbeck
Lingzhen Song
Mattia Chini
Sebastian H Bitzenhofer
Ileana L Hanganu-Opatz
author_facet Joachim Ahlbeck
Lingzhen Song
Mattia Chini
Sebastian H Bitzenhofer
Ileana L Hanganu-Opatz
author_sort Joachim Ahlbeck
collection DOAJ
description The long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactions is still unresolved. Here, we selectively target optogenetic manipulation of glutamatergic projection neurons in the CA1 area of either dorsal or intermediate/ventral hippocampus at neonatal age to elucidate their contribution to the emergence of prefrontal oscillatory entrainment. We show that despite stronger theta and ripples power in dorsal hippocampus, the prefrontal cortex is mainly coupled with intermediate/ventral hippocampus by phase-locking of neuronal firing via dense direct axonal projections. Theta band-confined activation by light of pyramidal neurons in intermediate/ventral but not dorsal CA1 that were transfected by in utero electroporation with high-efficiency channelrhodopsin boosts prefrontal oscillations. Our data causally elucidate the cellular origin of the long-range coupling in the developing brain.
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spelling doaj.art-a5e95be27d3c4d459fc63808fdb9fa7b2022-12-22T03:52:51ZengeLife Sciences Publications LtdeLife2050-084X2018-04-01710.7554/eLife.33158Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouseJoachim Ahlbeck0https://orcid.org/0000-0002-4439-0798Lingzhen Song1Mattia Chini2https://orcid.org/0000-0002-5782-9720Sebastian H Bitzenhofer3Ileana L Hanganu-Opatz4https://orcid.org/0000-0002-4787-1765Developmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, GermanyDevelopmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, GermanyDevelopmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, GermanyDevelopmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, GermanyDevelopmental Neurophysiology, Institute of Neuroanatomy, University Medical Center Hamburg-Eppendorf, Hamburg, GermanyThe long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactions is still unresolved. Here, we selectively target optogenetic manipulation of glutamatergic projection neurons in the CA1 area of either dorsal or intermediate/ventral hippocampus at neonatal age to elucidate their contribution to the emergence of prefrontal oscillatory entrainment. We show that despite stronger theta and ripples power in dorsal hippocampus, the prefrontal cortex is mainly coupled with intermediate/ventral hippocampus by phase-locking of neuronal firing via dense direct axonal projections. Theta band-confined activation by light of pyramidal neurons in intermediate/ventral but not dorsal CA1 that were transfected by in utero electroporation with high-efficiency channelrhodopsin boosts prefrontal oscillations. Our data causally elucidate the cellular origin of the long-range coupling in the developing brain.https://elifesciences.org/articles/33158cortical developmentoptogeneticsoscillationsprefrontalhippocampal
spellingShingle Joachim Ahlbeck
Lingzhen Song
Mattia Chini
Sebastian H Bitzenhofer
Ileana L Hanganu-Opatz
Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
eLife
cortical development
optogenetics
oscillations
prefrontal
hippocampal
title Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
title_full Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
title_fullStr Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
title_full_unstemmed Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
title_short Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
title_sort glutamatergic drive along the septo temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse
topic cortical development
optogenetics
oscillations
prefrontal
hippocampal
url https://elifesciences.org/articles/33158
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