Skewed distribution of spines is independent of presynaptic transmitter release and synaptic plasticity and emerges early during adult neurogenesis

Roessler, Nina; Jungenitz, Tassilo; Sigler, Albrecht; Bird, Alexander; Mittag, Martin; Rhee, Jeong−Seop; Deller, Thomas; Cuntz, Hermann; Schwarzacher, Stephan W.; Jedlicka, Paul

doi:10.1101/2023.03.15.532740

Cited by 3 publications

(2 citation statements)

References 77 publications

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“…Extreme distributions of firing rates and functional connectivity are also observed in human brain organoids 74,75 , that also do not have access to sensory inputs. Along the same lines, in vivo blocking of synaptic transmission in the hippocampus of anesthetized rats does not alter the distribution of spine sizes 76 . Even more surprisingly, completely abolishing all central nervous system activity for the first four days of life of the larval zebrafish only minimally impacts the tuning and functionality of neurons, and the ability of the fish to learn a complex visuomotor task 72 .…”

Section: Discussionmentioning

confidence: 93%

“…Third, while our results argue against a role of experience in shaping these processes, we do provide an alternative mechanistic answer to the question. This topic has however already been the subject of a number of theoretical studies 7,9,76,89 . Further, we generated a large and detailed experimental open-access database that could be instrumental in benchmarking future research on this topic.…”

Section: Discussionmentioning

confidence: 99%

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Extreme distributions in the preconfigured developing brain

Chini,

Hnida,

Kostka

et al. 2023

Preprint

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In the adult brain, structural and functional parameters, such as synaptic sizes and neuronal firing rates, follow right-skewed and heavy-tailed distributions. While this organization is thought of having significant implications, its development is still largely unknown. Here, we address this knowledge gap by investigating a large-scale dataset recorded from the prefrontal cortex (PFC) and the olfactory bulb of mice aged 4-60 postnatal days. We show that firing rates and pairwise correlations have a largely stable distribution shape over age, and that neural activity displays a small-world architecture. Moreover, early brain activity displays an oligarchical organization, i.e., neurons with high firing rates are likely to have hub-like properties. Leveraging neural network modeling, we show that analogously extremely distributed synaptic parameters are necessary to recapitulate the experimental data. Thus, functional and structural parameters in the developing brain are already extremely distributed, suggesting that this organization is preconfigured and not experience-dependent.

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Section: Discussionmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Extreme distributions in the preconfigured developing brain

Chini,

Hnida,

Kostka

et al. 2023

Preprint

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Skewed distribution of spines is independent of presynaptic transmitter release and synaptic plasticity, and emerges early during adult neurogenesis

Rößler,

Jungenitz,

Sigler

et al. 2023

Open Biol.

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Dendritic spines are crucial for excitatory synaptic transmission as the size of a spine head correlates with the strength of its synapse. The distribution of spine head sizes follows a lognormal-like distribution with more small spines than large ones. We analysed the impact of synaptic activity and plasticity on the spine size distribution in adult-born hippocampal granule cells from rats with induced homo- and heterosynaptic long-term plasticity in vivo and CA1 pyramidal cells from Munc13–1/Munc13–2 knockout mice with completely blocked synaptic transmission. Neither the induction of extrinsic synaptic plasticity nor the blockage of presynaptic activity degrades the lognormal-like distribution but changes its mean, variance and skewness. The skewed distribution develops early in the life of the neuron. Our findings and their computational modelling support the idea that intrinsic synaptic plasticity is sufficient for the generation, while a combination of intrinsic and extrinsic synaptic plasticity maintains lognormal-like distribution of spines.

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Assemblies, synapse clustering and network topology interact with plasticity to explain structure-function relationships of the cortical connectome

Ecker,

Egas Santander,

Abdellah

et al. 2023

Preprint

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Synaptic plasticity underlies the brain’s ability to learn and adapt. This process is often studied in small groups of neuronsin vitroor indirectly through its effects on behaviorin vivo. Due to the limitations of available experimental techniques, investigating synaptic plasticity at the micro-circuit level relies on simulation-based approaches. Although modeling studies provide valuable insights, they are usually limited in scale and generality. To overcome these limitations, we extended a previously published and validated large-scale cortical network model with a recently developed calcium-based model of functional plasticity between excitatory cells. We calibrated the network to mimic anin vivostate characterized by low synaptic release probability and low-rate asynchronous firing, and exposed it to ten different stimuli. We found that synaptic plasticity sparsely and specifically strengthened synapses forming spatial clusters on postsynaptic dendrites and those between populations of co-firing neurons, also known as cell assemblies: among 312 million synapses, only 5% experienced noticeable plasticity and cross-assembly synapses underwent three times more changes than average. Furthermore, as occasional large-amplitude potentiation was counteracted by more frequent synaptic depression, the network remained stable without explicitly modeling homeostatic plasticity. When comparing the network’s responses to the different stimuli before and after plasticity, we found that it became more stimulus-specific after plasticity, manifesting in prolonged activity after selected stimuli and more unique groups of neurons responding exclusively to a single pattern. Taken together, we present the first stable simulation of Hebbian plasticity without homeostatic terms at this level of detail and analyze the rules determining the sparse changes.

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Skewed distribution of spines is independent of presynaptic transmitter release and synaptic plasticity and emerges early during adult neurogenesis

Cited by 3 publications

References 77 publications

Extreme distributions in the preconfigured developing brain

Extreme distributions in the preconfigured developing brain

Skewed distribution of spines is independent of presynaptic transmitter release and synaptic plasticity, and emerges early during adult neurogenesis

Assemblies, synapse clustering and network topology interact with plasticity to explain structure-function relationships of the cortical connectome

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