Temporal Embryonic Origin Critically Determines Cellular Physiology in the Dentate Gyrus

Save, Laurène; Baude, Agnès; Cossart, Rosa

doi:10.1093/cercor/bhy132

Cited by 44 publications

(67 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The putative depolarization block observed in ebGABA could result from the interplay between sodium and delayed rectifier potassium conductances 21 . Interestingly, a similarly lower intrinsic excitability was recently reported to distinguish granule cells with an early temporal embryonic origin 36 , suggesting that this may represent a common feature of early born cells, regardless of the neurotransmitter that they…”

Section: Discussionmentioning

confidence: 69%

Hippocampal hub neurons maintain unique functional properties throughout their lifetime

Bocchio

Gouny

Angulo-Garcia

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

The temporal embryonic origins of cortical GABA neurons are critical for their specialization. In the neonatal hippocampus, GABA cells born the earliest (ebGABAs) operate as 'hubs' by orchestrating neuronal dynamics. However, their fate remains largely unknown. To fill this gap, we have examined CA1 ebGABAs using a combination of electrophysiology, neurochemical analysis, optogenetic connectivity mapping as well as ex vivo and in vivo calcium imaging. We show that CA1 ebGABAs not only operate as hubs during development, but also maintain distinct morpho-physiological and connectivity profiles, including a bias for long-range targets and local excitatory inputs. In vivo, ebGABAs signal a variety of network states, including the activation of local CA1 assemblies. Hence, ebGABAs are specified from birth to ensure unique functions throughout their lifetime. In the adult brain, this may take the form of a long-range hub role through the coordination of cell assemblies across distant regions.

show abstract

Section: Discussionmentioning

confidence: 69%

Hippocampal hub neurons maintain unique functional properties throughout their lifetime

Bocchio

Gouny

Angulo-Garcia

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Their loss could also be due to extrinsic features; for example, the type of information that they store during their critical period may predispose them to turn over. E19-born cells, in contrast, could reflect specialized dentate gyrus cell populations (Kerloch et al, 2018;Save et al, 2018) that are more resistant to cell death. It is also likely that E19-generated neurons are very different from the majority of DG neurons since they undergo significant migration to reach their final destination.…”

Section: Discussionmentioning

confidence: 99%

“…Mature DG neurons are not identical and even cells born at different stages of perinatal development can have distinct properties (Kerloch, Clavreul, Goron, Abrous, & Pacary, 2018;Save, Baude, & Cossart, 2018;Snyder, 2019). Indeed, DG neurogenesis spans many developmental milestones that may differentially recruit new neurons and affect their survival phenotype (e.g., birth, eye opening, weaning).…”

mentioning

confidence: 99%

Dentate gyrus neurons that are born at the peak of development, but not before or after, die in adulthood

2019

View full text Add to dashboard Cite

IntroductionIn the dentate gyrus of the rodent hippocampus, neurogenesis begins prenatally and continues to the end of life. Adult‐born neurons often die in the first few weeks after mitosis, but those that survive to 1 month persist indefinitely. In contrast, neurons born at the peak of development are initially stable but can die later in adulthood. Physiological and pathological changes in the hippocampus may therefore result from both the addition of new neurons and the loss of older neurons. The extent of neuronal loss remains unclear since no studies have examined whether neurons born at other stages of development also undergo delayed cell death.MethodsWe used BrdU to label dentate granule cells that were born in male rats on embryonic day 19 (E19; before the developmental peak), postnatal day 6 (P6; peak), and P21 (after the peak). We quantified BrdU+ neurons in separate groups of rats at 2 and 6 months post‐BrdU injection to estimate cell death in young adulthood.ResultsConsistent with previous work, there was a 15% loss of P6‐born neurons between 2 and 6 months of age. In contrast, E19‐ or P21‐born neurons were stable throughout young adulthood.DiscussionDelayed death of P6‐born neurons suggests these cells may play a unique role in hippocampal plasticity adulthood, for example, by contributing to the turnover of hippocampal memory. Their loss may also play a role in disorders that are characterized by hippocampal atrophy.

show abstract

“…Mature DG neurons are not identical and even cells born at different stages of perinatal development can have distinct properties (Kerloch et al, 2018;Save et al, 2018;Snyder, 2019). Indeed, DG neurogenesis spans many developmental milestones that may differentially recruit new neurons and affect their survival phenotype (e.g.…”

mentioning

confidence: 99%

“…Assuming that there is a degree of functional heterogeneity within the DG that depends on when a cell was born (Snyder, 2019), P6-born cells may be reflective of the largest cohort of DG neurons, and therefore may be the most dispensable. Possibly, E19-born cells reflect specialized dentate gyrus cell populations (Kerloch et al, 2018;Save et al, 2018), which render them more resistant to cell death. It is also likely that E19-generated neurons are very different from the majority of DG neurons since they undergo significant migration to reach their final destination.…”

mentioning

confidence: 99%

Dentate gyrus neurons that are born at the peak of development, but not before or after, die in adulthood

Ciric

Cahill

Snyder

2019

Preprint

View full text Add to dashboard Cite

Introduction In the dentate gyrus of the rodent hippocampus, neurogenesis begins prenatally and continues to the end of life. Adult‐born neurons often die in the first few weeks after mitosis, but those that survive to 1 month persist indefinitely. In contrast, neurons born at the peak of development are initially stable but can die later in adulthood. Physiological and pathological changes in the hippocampus may therefore result from both the addition of new neurons and the loss of older neurons. The extent of neuronal loss remains unclear since no studies have examined whether neurons born at other stages of development also undergo delayed cell death. Methods We used BrdU to label dentate granule cells that were born in male rats on embryonic day 19 (E19; before the developmental peak), postnatal day 6 (P6; peak), and P21 (after the peak). We quantified BrdU+ neurons in separate groups of rats at 2 and 6 months post‐BrdU injection to estimate cell death in young adulthood. Results Consistent with previous work, there was a 15% loss of P6‐born neurons between 2 and 6 months of age. In contrast, E19‐ or P21‐born neurons were stable throughout young adulthood. Discussion Delayed death of P6‐born neurons suggests these cells may play a unique role in hippocampal plasticity adulthood, for example, by contributing to the turnover of hippocampal memory. Their loss may also play a role in disorders that are characterized by hippocampal atrophy.

show abstract

Temporal Embryonic Origin Critically Determines Cellular Physiology in the Dentate Gyrus

Cited by 44 publications

References 48 publications

Hippocampal hub neurons maintain unique functional properties throughout their lifetime

Hippocampal hub neurons maintain unique functional properties throughout their lifetime

Dentate gyrus neurons that are born at the peak of development, but not before or after, die in adulthood

Dentate gyrus neurons that are born at the peak of development, but not before or after, die in adulthood

Contact Info

Product

Resources

About