Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers

Zhao, Chen; Jou, Jessica; Wolff, Lisa J.; Sun, Hongbo; Gage, Fred H.

doi:10.1002/cne.23581

Cited by 45 publications

(31 citation statements)

References 27 publications

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“…Interestingly, the heightened excitatory response in PAE‐EE mice was not associated with increased spine density. Previous studies have shown that neither EE, nor exercise, has a significant impact on total spine density in aDGCs, although both promote increased density of mushroom spines, which are thought to represent sites of enhanced excitatory synaptic transmission (Zhao et al, ; Piatti et al, ; Zhao et al, ). On the other hand, training on discrete spatial tasks stimulates enhanced dendritic complexity and spine density in aDGCs in proportion to the intensity of cognitive demand (Tronel et al, ; Lemaire et al, ).…”

Section: Discussionmentioning

confidence: 99%

Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment

et al. 2016

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Prenatal alcohol exposure (PAE) results in fetal alcohol spectrum disorder (FASD), which is characterized by a wide range of cognitive and behavioral deficits that may be linked to impaired hippocampal function and adult neurogenesis. Preclinical studies in mouse models of FASD indicate that PAE markedly attenuates enrichment-mediated increases in the number of adult-generated hippocampal dentate granule cells (aDGCs), but whether synaptic activity is also affected has not been studied. Here, we utilized retroviral birth-dating coupled with whole cell patch electrophysiological recordings to assess the effects of PAE on enrichment-mediated changes in excitatory and inhibitory synaptic activity as a function of DGC age. We found that exposure to an enriched environment (EE) had no effect on baseline synaptic activity of 4 week or 8 week old aDGCs from control mice, but significantly enhanced the excitatory/inhibitory ratio of synaptic activity in 8 week old aDGCs from PAE mice. In contrast, exposure to EE significantly enhanced the excitatory/inhibitory ratio of synaptic activity in older pre-existing DGCs situated in the outer dentate granule cell layer (i.e., those generated during embryonic development; dDGCs) in control mice, an effect that was blunted in PAE mice. These findings indicate distinct electrophysiological responses of hippocampal DGCs to behavioral challenge based on cellular ontogenetic age, and suggest that PAE disrupts EE-mediated changes in overall hippocampal network activity. These findings may have implications for future therapeutic targeting of hippocampal dentate circuitry in clinical FASD.

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Section: Discussionmentioning

confidence: 99%

Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment

et al. 2016

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“…In addition, dendritic spine motility, total dendritic length, branch points, dendritic complexity, and mitochondria density are significantly higher in runners’ adult-born DG neurons for up to 3 weeks post-retroviral injection (Zhao et al 2006; Dietrich et al 2008; Steib et al 2014). However, by the fourth week, dendritic morphology and mitochondria content are indistinguishable from adult-born DG neurons in the sedentary brain (Zhao et al 2006, 2014; Steib et al 2014). Similar observations were made in a live imaging study in mice housed in an enriched environment containing running wheels (Gonçalves et al 2016).…”

Section: Exercise and The Hippocampusmentioning

confidence: 96%

“…Running may shorten the cell cycle of rapidly amplifying progenitor cells (Farioli-Vecchioli et al 2014; see, however, Fischer et al 2014) and accelerate neuronal maturation of adult-born DG neurons (Zhao et al 2006; Piatti et al 2011; Steib et al 2014). In particular, retroviral labeling studies (van Praag et al 2002; Zhao et al 2006) have shown that running promotes spine formation in the outer molecular layer of adult-born dentate granule cell dendrites (Zhao et al 2014). In addition, dendritic spine motility, total dendritic length, branch points, dendritic complexity, and mitochondria density are significantly higher in runners’ adult-born DG neurons for up to 3 weeks post-retroviral injection (Zhao et al 2006; Dietrich et al 2008; Steib et al 2014).…”

Section: Exercise and The Hippocampusmentioning

confidence: 99%

On the Run for Hippocampal Plasticity

Cooper

Moon

Praag

2017

Cold Spring Harb Perspect Med

120

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Accumulating research in rodents and humans indicates that exercise benefits brain function and may prevent or delay onset of neurodegenerative conditions. In particular, exercise modifies the structure and function of the hippocampus, a brain area important for learning and memory. This review addresses the central and peripheral mechanisms underlying the beneficial effects of exercise on the hippocampus. We focus on running-induced changes in adult hippocampal neurogenesis, neural circuitry, neurotrophins, synaptic plasticity, neurotransmitters, and vasculature. The role of peripheral factors in hippocampal plasticity is also highlighted. We discuss recent evidence that systemic factors released from peripheral organs such as muscle (myokines), liver (hepatokines), and adipose tissue (adipokines) during exercise contribute to hippocampal neurotrophin and neurogenesis levels, and memory function. A comprehensive understanding of the body–brain axis is needed to elucidate how exercise improves hippocampal plasticity and cognition.

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“…Spatial cues induce mushroom spine formation in the middle molecular layer of newborn neurons that receive inputs from the entorhinal cortex (EC) providing spatial information. Conversely, non-spatial components increase mushroom spine formation in the outer molecular layer receiving inputs from the lateral EC (Zhao et al 2014). Voluntary exercise affects dendritic complexity and spine density not only in the DG but also in afferent populations like pyramidal neurons in the CA1 and layer III pyramidal neurons of the entorhinal cortex (Redila and Christie 2006;Stranahan et al 2007).…”

Section: Exercise and Enriched Environment In Animals: From Cognitionmentioning

confidence: 98%

Role of Adult Hippocampal Neurogenesis in Cognition in Physiology and Disease: Pharmacological Targets and Biomarkers

Costa

Lugert

Jagasia

2015

Handbook of Experimental Pharmacology

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Adult hippocampal neurogenesis is a remarkable form of brain structural plasticity by which new functional neurons are generated from adult neural stem cells/precursors. Although the precise role of this process remains elusive, adult hippocampal neurogenesis is important for learning and memory and it is affected in disease conditions associated with cognitive impairment, depression, and anxiety. Immature neurons in the adult brain exhibit an enhanced structural and synaptic plasticity during their maturation representing a unique population of neurons to mediate specific hippocampal function. Compelling preclinical evidence suggests that hippocampal neurogenesis is modulated by a broad range of physiological stimuli which are relevant in cognitive and emotional states. Moreover, multiple pharmacological interventions targeting cognition modulate adult hippocampal neurogenesis. In addition, recent genetic approaches have shown that promoting neurogenesis can positively modulate cognition associated with both physiology and disease. Thus the discovery of signaling pathways that enhance adult neurogenesis may lead to therapeutic strategies for improving memory loss due to aging or disease. This chapter endeavors to review the literature in the field, with particular focus on (1) the role of hippocampal neurogenesis in cognition in physiology and disease; (2) extrinsic and intrinsic signals that modulate hippocampal neurogenesis with a focus on pharmacological targets; and (3) efforts toward novel strategies pharmacologically targeting neurogenesis and identification of biomarkers of human neurogenesis.

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Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers

Cited by 45 publications

References 27 publications

Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment

Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment

On the Run for Hippocampal Plasticity

Role of Adult Hippocampal Neurogenesis in Cognition in Physiology and Disease: Pharmacological Targets and Biomarkers

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