Entorhinal Denervation Induces Homeostatic Synaptic Scaling of Excitatory Postsynapses of Dentate Granule Cells in Mouse Organotypic Slice Cultures

Vlachos, Andreas; Becker, Denise; Jedlicka, Paul; Winkels, Raphael; Roeper, Jochen; Deller, Thomas

doi:10.1371/journal.pone.0032883

Cited by 50 publications

(98 citation statements)

References 72 publications

(105 reference statements)

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“…Based on this result, we conclude that immature dentate GCs are capable of increasing their excitatory synaptic strength in a compensatory manner, similar to what is observed in mature cultured dentate GCs (Vlachos et al, 2012). …”

Section: Resultssupporting

confidence: 88%

Dopamine Modulates Homeostatic Excitatory Synaptic Plasticity of Immature Dentate Granule Cells in Entorhino-Hippocampal Slice Cultures

Strehl

Galanis

Radic

et al. 2018

Front. Mol. Neurosci.

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Homeostatic plasticity mechanisms maintain neurons in a stable state. To what extent these mechanisms are relevant during the structural and functional maturation of neural tissue is poorly understood. To reveal developmental changes of a major homeostatic plasticity mechanism, i.e., homeostatic excitatory synaptic plasticity, we analyzed 1-week- and 4-week-old entorhino-hippocampal slice cultures and investigated the ability of immature and mature dentate granule cells (GCs) to express this form of plasticity. Our experiments demonstrate that immature GCs are capable of adjusting their excitatory synaptic strength in a compensatory manner at early postnatal stages, i.e., in 1-week-old preparations, as is the case for mature GCs. This ability of immature dentate GCs is absent in 4-week-old slice cultures. Further investigations into the signaling pathways reveal an important role of dopamine (DA), which prevents homeostatic synaptic up-scaling of immature GCs in young cultures, whereas it does not affect immature and mature GCs in 4-week-old preparations. Together, these results disclose the ability of immature GCs to express homeostatic synaptic plasticity during early postnatal development. They hint toward a novel role of dopaminergic signaling, which may gate activity-dependent changes of newly born neurons by blocking homeostasis.

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Section: Resultssupporting

confidence: 88%

Dopamine Modulates Homeostatic Excitatory Synaptic Plasticity of Immature Dentate Granule Cells in Entorhino-Hippocampal Slice Cultures

Strehl

Galanis

Radic

et al. 2018

Front. Mol. Neurosci.

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“…To the best of our knowledge, this is the first report about the properties of the ongoing MCs activity in the deprived OB. Interestingly, our results are consistent with the homeostatic regulation of the OB circuitry that adjust the level of baseline activity to different levels of external drive [41].…”

Section: Discussionsupporting

confidence: 88%

Neural Sensitivity to Odorants in Deprived and Normal Olfactory Bulbs

2013

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Early olfactory deprivation in rodents is accompanied by an homeostatic regulation of the synaptic connectivity in the olfactory bulb (OB). However, its consequences in the neural sensitivity and discrimination have not been elucidated. We compared the odorant sensitivity and discrimination in early sensory deprived and normal OBs in anesthetized rats. We show that the deprived OB exhibits an increased sensitivity to different odorants when compared to the normal OB. Our results indicate that early olfactory stimulation enhances discriminability of the olfactory stimuli. We found that deprived olfactory bulbs adjusts the overall excitatory and inhibitory mitral cells (MCs) responses to odorants but the receptive fields become wider than in the normal olfactory bulbs. Taken together, these results suggest that an early natural sensory stimulation sharpens the receptor fields resulting in a larger discrimination capability. These results are consistent with previous evidence that a varied experience with odorants modulates the OB's synaptic connections and increases MCs selectivity.

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“…Studies of weaver mice, which lack presynaptic parallel fibers, indicate that dendritic spines can form on deafferented cerebellar Purkinje cells (Hirano and Dembitzer, 1973; Sotelo, 1990). Similarly, in vitro denervation of mature granule cells in organotypic entorhino-hippocampal cultures, did not affect new spine formation, but the authors observed changes in spine stability and synaptic activity (Vlachos et al, 2012a; 2012b). In our in vivo experiments, there was no evidence of intact presynaptic terminals in the denervated zone at 21 days post-lesion.…”

Section: Discussionmentioning

confidence: 96%

Neural Injury Alters Proliferation and Integration of Adult-Generated Neurons in the Dentate Gyrus

et al. 2013

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Neural plasticity following brain injury illustrates the potential for regeneration in the central nervous system. Lesioning of the perforant path, which innervates the outer 2/3rds of the molecular layer of the dentate gyrus, was one of the first models to demonstrate structural plasticity of mature granule cells (Parnavelas, 1974; Caceres and Steward, 1983; Diekmann et al., 1996). The dentate gyrus also harbors a continuously proliferating population of neuronal precursors that can integrate into functional circuits and show enhanced short-term plasticity (Schmidt-Hieber et al., 2004; Abrous et al., 2005). To examine the response of adult-generated granule cells to unilateral complete transection of the perforant path in vivo, we tracked these cells using transgenic POMC-EGFP mice or by retroviral expression of GFP. Lesioning triggered a marked proliferation of newborn neurons. Subsequently, the dendrites of newborn neurons showed reduced complexity within the denervated zone, but dendritic spines still formed in the absence of glutamatergic nerve terminals. Electron micrographs confirmed the lack of intact presynaptic terminals apposing spines on mature cells and on newborn neurons. Newborn neurons, but not mature granule cells, had a higher density of dendritic spines in the inner molecular layer post-lesion, accompanied by an increase in miniature EPSC amplitudes and rise times. Our results indicate that injury causes an increase in newborn neurons and lamina-specific synaptic reorganization, indicative of enhanced plasticity. The presence of de novo dendritic spines in the denervated zone suggests that the post-lesion environment provides the necessary signals for spine formation.

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Entorhinal Denervation Induces Homeostatic Synaptic Scaling of Excitatory Postsynapses of Dentate Granule Cells in Mouse Organotypic Slice Cultures

Cited by 50 publications

References 72 publications

Dopamine Modulates Homeostatic Excitatory Synaptic Plasticity of Immature Dentate Granule Cells in Entorhino-Hippocampal Slice Cultures

Dopamine Modulates Homeostatic Excitatory Synaptic Plasticity of Immature Dentate Granule Cells in Entorhino-Hippocampal Slice Cultures

Neural Sensitivity to Odorants in Deprived and Normal Olfactory Bulbs

Neural Injury Alters Proliferation and Integration of Adult-Generated Neurons in the Dentate Gyrus

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