Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3

Jones, Shawn P.; Rahimi, Omid B.; O’Boyle, Michael; Diaz, Daniel L.; Claiborne, Brenda J.

doi:10.1002/hipo.10121

Cited by 84 publications

(85 citation statements)

References 61 publications

(96 reference statements)

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“…Thus, they showed that from the superficial granule cells, several dendrites, including apical and basal dendrites, grow into the surrounding neuropil, and that these dendrites have the classical appearance of growing dendrites, including lamellipodia and filopodia as described previously (Seress and Pokorny, 1981;Lubbers and Frotscher, 1988). It was also shown that the basal dendrites regress because they are a transient feature of granule cells during their development and adult rodent granule cells never display basal dendrites (Jones et al, 2003). Consistent with previous developmental studies, dendritic arbors become pruned to form only a few apical dendrites that branch in regular ways in the molecular layer Desmond and Levy, 1984;Green and Juraska, 1985;Rihn and Claiborne, 1990).…”

Section: Introductionsupporting

confidence: 54%

“…Also, they showed that in all regions of the dentate gyrus, the more superficial neurons in the granule cell layer are formed earlier than the deeper granule cells. In the early postnatal dentate gyrus, Jones et al (2003) have described a multipolar morphology for the developing dendrites of granule cells. Thus, they showed that from the superficial granule cells, several dendrites, including apical and basal dendrites, grow into the surrounding neuropil, and that these dendrites have the classical appearance of growing dendrites, including lamellipodia and filopodia as described previously (Seress and Pokorny, 1981;Lubbers and Frotscher, 1988).…”

Section: Introductionmentioning

confidence: 99%

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Dendritic development of newly generated neurons in the adult brain

Ribak¹,

Shapiro²

2007

Brain Research Reviews

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Ramon y Cajal described the fundamental morphology of the dendritic and axonal growth cones of neurons during development. However, technical limitations at the time prevented him from describing such growth cones from newborn neurons in the adult brain. The phenomenon of adult neurogenesis is briefly reviewed, and the structural description of dendritic and axonal outgrowth for these newly generated neurons in the adult brain is discussed. Axonal outgrowth into the hilus and CA3 region of the hippocampus occurs later than the outgrowth of dendrites into the molecular layer, and the ultrastructural analysis of axonal outgrowth has yet to be completed. In contrast, growth cones on dendrites from newborn neurons in the adult dentate gyrus have been described and this observation suggests that dendrites in adult brains grow in a similar way to those found in immature brains. However, dendrites in adult brains have to navigate through a denser neuropil and a more complex cell layer. Therefore, some aspects of dendritic outgrowth of neurons born in the adult dentate gyrus are different as compared to that found in development. These differences include the radial process of radial glial cells acting as a lattice to guide apical dendritic growth through the granule cell layer and a much thinner dendrite to grow through the neuropil of the molecular layer. Therefore, similarities and differences exist for dendritic outgrowth from newborn neurons in the developing and adult brain.

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Section: Introductionsupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Dendritic development of newly generated neurons in the adult brain

Ribak¹,

Shapiro²

2007

Brain Research Reviews

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“…Notably, 4-week-old granule cells are generally considered to be functionally mature (Markakis and Gage, 1999;Liu et al, 2000;Jones et al, 2003;Ambrogini et al, 2004;Espó sito et al, 2005;OverstreetWadiche et al, 2006a;Zhao et al, 2006). GFP expression in these animals therefore provides an efficient means to examine the morphology of mature hippocampal dentate granule cells.…”

Section: Gfp-expressing Neurons (0 Of 832 Cells)mentioning

confidence: 99%

Pilocarpine-Induced Seizures Cause Selective Time-Dependent Changes to Adult-Generated Hippocampal Dentate Granule Cells

Walter¹,

Murphy²,

Pun³

et al. 2007

J. Neurosci.

162

176

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Aberrantly interconnected granule cells are characteristic of temporal lobe epilepsy. By reducing network stability, these abnormal neurons may contribute directly to disease development. Only subsets of granule cells, however, exhibit abnormalities. Why this is the case is not known. Ongoing neurogenesis in the adult hippocampus may provide an explanation. Newly generated granule cells may be uniquely vulnerable to environmental disruptions relative to their mature neighbors. Here, we determine whether there is a critical period after neuronal birth during which neuronal integration can be disrupted by an epileptogenic insult. By bromodeoxyuridine birthdating cells in green fluorescent protein-expressing transgenic mice, we were able to noninvasively label granule cells born 8 weeks before (mature), 1 week before (immature), or 3 weeks after (newborn) pilocarpineepileptogenesis. Neuronal morphology was examined 4 and 8 weeks after pilocarpine treatment. Strikingly, almost 50% of immature granule cells exposed to pilocarpine-epileptogenesis exhibited aberrant hilar basal dendrites. In contrast, only 9% of mature granule cells exposed to the identical insult possessed basal dendrites. Moreover, newborn cells were even more severely impacted than immature cells, with 40% exhibiting basal dendrites and an additional 20% exhibiting migration defects. In comparison, Ͻ5% of neurons from normal animals exhibited either abnormality, regardless of age. Together, these data demonstrate the existence of a critical period after the birth of adult-generated neurons during which they are vulnerable to being recruited into epileptogenic neuronal circuits. Pathological brain states therefore may pose a significant hurdle for the appropriate integration of newly born endogenous, and exogenous, neurons.

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“…In addition, it needs to migrate, mature, and establish presynaptic and postsynaptic connections. In the developing hippocampus, this process has been studied extensively (Lübbers and Frotscher, 1988;Laurie et al, 1992;Super and Soriano, 1994;Tyzio et al, 1999;Hennou et al, 2002;Gozlan and Ben Ari, 2003;Jones et al, 2003), but the sequence of events leading to neuronal maturation in the adult hippocampus remains unknown. Given the differences in the developing and adult environments, the process of maturation and the factors that modulate it may also differ.…”

Section: Introductionmentioning

confidence: 99%

Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development

Esposito

Piatti²,

Laplagne³

et al. 2005

J. Neurosci.

593

674

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In the adult hippocampus and olfactory bulb, neural progenitor cells generate neurons that functionally integrate into the existing circuits. To understand how neuronal differentiation occurs in the adult hippocampus, we labeled dividing progenitor cells with a retrovirus expressing green fluorescent protein and studied the morphological and functional properties of their neuronal progeny over the following weeks. During the first week neurons had an irregular shape and immature spikes and were synaptically silent. Slow GABAergic synaptic inputs first appeared during the second week, when neurons exhibited spineless dendrites and migrated into the granule cell layer. In contrast, glutamatergic afferents were detected by the fourth week in neurons displaying mature excitability and morphology. Interestingly, fast GABAergic responses were the latest to appear. It is striking that neuronal maturation in the adult hippocampus follows a precise sequence of connectivity (silent 3 slow GABA 3 glutamate 3 fast GABA) that resembles hippocampal development. We conclude that, unlike what is observed in the olfactory bulb, the hippocampus maintains the same developmental rules for neuronal integration through adulthood.

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Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3

Cited by 84 publications

References 61 publications

Dendritic development of newly generated neurons in the adult brain

Dendritic development of newly generated neurons in the adult brain

Pilocarpine-Induced Seizures Cause Selective Time-Dependent Changes to Adult-Generated Hippocampal Dentate Granule Cells

Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development

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