Hippocampal Neurogenesis Regulates Forgetting During Adulthood and Infancy

Akers, Katherine G.; Martínez-Canabal, Alonso; Restivo, Leonardo; Yiu, Adelaide P.; Cristofaro, Antonietta De; Hsiang, Hwa-Lin Liz; Wheeler, Anne L.; Guskjolen, Axel; Niibori, Yosuke; Shoji, Hirotaka; Ohira, Koji; Richards, Blake A; Miyakawa, Tsuyoshi; Josselyn, Sheena A.; Frankland, Paul W.

doi:10.1126/science.1248903

Cited by 631 publications

(611 citation statements)

References 56 publications

(49 reference statements)

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“…This theory generally fits with the data presented in Freund et al (2013): animals with lower levels of neurogenesis have lower cRE values at T4, i.e., they moved in a more predictable way. This would suggest that adult hippocampal neurogenesis retains the brain in a certain ''juvenile'' reserve, thus providing it with a wider range of behavioral opportunities (Altman et al, 1973;Kempermann, 2008;Amrein and Lipp, 2009;Akers et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Association between exploratory activity and social individuality in genetically identical mice living in the same enriched environment

et al. 2015

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Abstract-We previously reported that inbred, genetically identical mice living in one enriched environment develop individual behavioral trajectories, indicating increasingly different levels of spatial exploratory behavior as quantified by roaming entropy. Cumulative roaming entropy (cRE) correlated positively with adult hippocampal neurogenesis, a type of plasticity involved in the flexible integration of new information into existing contexts (Freund et al., 2013). The study on which we report here was done in parallel to that first experiment, but here we acquired detailed observational data on the behavior of individual mice. Roaming entropy (RE) was again assessed in real-time with an antenna-based system over the entire experimental period of 3 months. Compared to the least active mice in the enclosure (low number of antenna contacts), the most active animals showed tendencies of increased socially interactive behavior in the final observation block whereas least active mice displayed more self-related behavior (non-social local exploration and play). When looking at roaming behavior, we discovered that RE correlated negatively with latent factors representing social exploratory and non-social exploratory and play behavior. Adult neurogenesis could not be studied in the present cohort but we do know that under identical conditions, cumulative RE correlated positively with adult hippocampal neurogenesis. We can thus hypothesize that the mice with more exploratory experience in terms of areal coverage (as quantified by RE) and related greater levels of adult hippocampal plasticity, might also be the ones that were less involved in interactions within the group and, hence, more individualistic. While this remains to be confirmed experimentally, the present data suggest that the described mechanism of individualization, which has previously been shown to be hippocampus-dependent, has a social component.

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Section: Discussionmentioning

confidence: 99%

Association between exploratory activity and social individuality in genetically identical mice living in the same enriched environment

et al. 2015

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“…The emergence of contextual fear learning may reflect increased maturation of the hippocampus and its connections to the amygdala in the post-weanling animals (Raineki et al, 2010). Contextual fear memories in this juvenile, pre-adolescent phase are also labile, and undergo forgetting with the passage of time (Akers et al, 2014). This infantile amnesia stems from heightened hippocampal neurogenesis, which is thought to induce reconfiguration of the neural circuits that encode hippocampal-dependent memories (Akers et al, 2014).…”

Section: Developmental Changes In Fear-learning Circuitsmentioning

confidence: 99%

“…Contextual fear memories in this juvenile, pre-adolescent phase are also labile, and undergo forgetting with the passage of time (Akers et al, 2014). This infantile amnesia stems from heightened hippocampal neurogenesis, which is thought to induce reconfiguration of the neural circuits that encode hippocampal-dependent memories (Akers et al, 2014). In contrast, during adolescence, once contextual fear learning is acquired, its expression undergoes a temporary suppression (Pattwell et al, 2011).…”

Section: Developmental Changes In Fear-learning Circuitsmentioning

confidence: 99%

Sensitive Periods in Affective Development: Nonlinear Maturation of Fear Learning

Hartley

Lee

2014

Neuropsychopharmacol

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At specific maturational stages, neural circuits enter sensitive periods of heightened plasticity, during which the development of both brain and behavior are highly receptive to particular experiential information. A relatively advanced understanding of the regulatory mechanisms governing the initiation, closure, and reinstatement of sensitive period plasticity has emerged from extensive research examining the development of the visual system. In this article, we discuss a large body of work characterizing the pronounced nonlinear changes in fear learning and extinction that occur from childhood through adulthood, and their underlying neural substrates. We draw upon the model of sensitive period regulation within the visual system, and present burgeoning evidence suggesting that parallel mechanisms may regulate the qualitative changes in fear learning across development.

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“…As a follow-up study in a later model, they examined the effect of neurogenesis on forgetting within their 2009 model, indicating the new neurons help the system eliminate older memories from the system . Notably, their prediction that new neurons are useful for forgetting was supported by recent evidence from the Frankland laboratory (Akers et al 2014). …”

Section: The Neurogenic Hippocampusmentioning

confidence: 86%

Computational Modeling of Adult Neurogenesis

Aimone¹

2016

Cold Spring Harb Perspect Biol

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The restriction of adult neurogenesis to only a handful of regions of the brain is suggestive of some shared requirement for this dramatic form of structural plasticity. However, a common driver across neurogenic regions has not yet been identified. Computational studies have been invaluable in providing insight into the functional role of new neurons; however, researchers have typically focused on specific scales ranging from abstract neural networks to specific neural systems, most commonly the dentate gyrus area of the hippocampus. These studies have yielded a number of diverse potential functions for new neurons, ranging from an impact on pattern separation to the incorporation of time into episodic memories to enabling the forgetting of old information. This review will summarize these past computational efforts and discuss whether these proposed theoretical functions can be unified into a common rationale for why neurogenesis is required in these unique neural circuits.T he importance of neurogenesis will be ultimately tied to its impact on the computational function of the overall circuit within which it resides. Notably, the two mammalian regions where neurogenesis is typically studied, the olfactory bulb (OB) and the dentate gyrus (DG) region of the hippocampus, have considerably different functions. The OB is a primary sensory region, essentially the equivalent of the processing layers of the retina, providing an initial transformation of raw olfactory inputs to the brain. In contrast, the hippocampus is one of the deepest structures in the brain, residing many layers away from sensory inputs and vital for episodic memory formation.Interestingly, as noted throughout this collection, although OB and DG neurogenesis share some similarities, there are sufficient differences to make it difficult to generalize across the two systems, not the least of which is the recent observation that humans likely lack OB neurogenesis. This is somewhat supported by a comparative perspective. As with mammals, neurogenesis in birds is limited to several structures with certain species, including neurogenesis in well-studied birdsong regions. Vertebrates with arguably less advanced nervous systems, such as reptiles and fish, have more widespread neurogenesis, suggesting that broad evolutionary pressures to attenuate neurogenesis in other areas of the brain led to the relative isolation of the OB and hippocampus as opposed to an evolutionary gain-of-function process common to the OB and DG. This subtle distinction has implications on how far one can hope for a shared function between these areas and, for this reason, it is not surprising that most computational studies investigating

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Hippocampal Neurogenesis Regulates Forgetting During Adulthood and Infancy

Cited by 631 publications

References 56 publications

Association between exploratory activity and social individuality in genetically identical mice living in the same enriched environment

Association between exploratory activity and social individuality in genetically identical mice living in the same enriched environment

Sensitive Periods in Affective Development: Nonlinear Maturation of Fear Learning

Computational Modeling of Adult Neurogenesis

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