Impact of functional synapse clusters on neuronal response selectivity

Ujfalussy, Balázs; Makara, Judit K.

doi:10.1038/s41467-020-15147-6

Cited by 39 publications

(24 citation statements)

References 78 publications

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“…By using randomly distributed inputs, our results suggest that functional synaptic clusters may emerge from potentiating neighboring synapses that each receive higher than average input. Our results are consistent with another modeling study investigating the impact of synaptic clustering on somatic membrane potential with in vivo-like conditions [ 93 ], which suggested that global plasticity rules would not be sufficient for formation of synaptic clusters. Our data-driven model of calcium dynamics accounts for global processes (produced by somatic spiking) and local processes (such as NMDA spikes), and the calcium-based synaptic plasticity rule can produce spatial clustering.…”

Section: Discussionsupporting

confidence: 92%

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Dorman

Blackwell

2022

Biomolecules

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Synaptic plasticity, the experience-induced change in connections between neurons, underlies learning and memory in the brain. Most of our understanding of synaptic plasticity derives from in vitro experiments with precisely repeated stimulus patterns; however, neurons exhibit significant variability in vivo during repeated experiences. Further, the spatial pattern of synaptic inputs to the dendritic tree influences synaptic plasticity, yet is not considered in most synaptic plasticity rules. Here, we investigate how spatiotemporal synaptic input patterns produce plasticity with in vivo-like conditions using a data-driven computational model with a plasticity rule based on calcium dynamics. Using in vivo spike train recordings as inputs to different size clusters of spines, we show that plasticity is strongly robust to trial-to-trial variability of spike timing. In addition, we derive general synaptic plasticity rules describing how spatiotemporal patterns of synaptic inputs control the magnitude and direction of plasticity. Synapses that strongly potentiated have greater firing rates and calcium concentration later in the trial, whereas strongly depressing synapses have hiring firing rates early in the trial. The neighboring synaptic activity influences the direction and magnitude of synaptic plasticity, with small clusters of spines producing the greatest increase in synaptic strength. Together, our results reveal that calcium dynamics can unify diverse plasticity rules and reveal how spatiotemporal firing rate patterns control synaptic plasticity.

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Section: Discussionsupporting

confidence: 92%

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Dorman

Blackwell

2022

Biomolecules

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“…Computational and in vitro studies indicate that 10–20 synchronized inputs are required to trigger dendritic spikes ( Ujfalussy and Makara, 2020 ). Existing in vivo studies, however, have found synchrony in only up to five neighboring dendritic spines, making it unclear what the impact of the synaptic clusters on the membrane potential of the posysynaptic neuron might be.…”

Section: Discussionmentioning

confidence: 99%

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Ashaber

Tomina

Kassraian

et al. 2021

eLife

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Dorsal Excitor motor neuron DE-3 in the medicinal leech plays three very different dynamical roles in three different behaviors. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play appropriate roles in various behaviors? We previously used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the leech segmental ganglion during (fictive) swimming, crawling, and local-bend escape (Tomina and Wagenaar, 2017). Here, we repeated that experiment, then re-imaged the same ganglion using serial blockface electron microscopy and traced DE-3's processes. Further, we traced back the processes of DE-3's presynaptic partners to their respective somata. This allowed us to analyze the relationship between circuit anatomy and the activity patterns it sustains. We found that input synapses important for all of the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.

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“…Dendrites can support information processing at multiple spatial scales ( ). On the local scale, i.e., the fine-scale organization of synapses over tens of microns, dendrites affect information processing by organizing synapses with similar properties into synaptic clusters that boost a neuron’s computational capacity through nonlinear integration ( ; , ; ; ; ). On the level of individual branches, dendrites exhibit dendritic maps in which the tuning of synapses (or synaptic clusters) varies systematically across the dendritic tree ( ; ; ; ; ).…”

Section: Organization Of Excitatory Synapsesmentioning

confidence: 99%

Emergence of synaptic organization and computation in dendrites

Kirchner

Gjorgjieva

2021

Neuroforum

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Single neurons in the brain exhibit astounding computational capabilities, which gradually emerge throughout development and enable them to become integrated into complex neural circuits. These capabilities derive in part from the precise arrangement of synaptic inputs on the neurons’ dendrites. While the full computational benefits of this arrangement are still unknown, a picture emerges in which synapses organize according to their functional properties across multiple spatial scales. In particular, on the local scale (tens of microns), excitatory synaptic inputs tend to form clusters according to their functional similarity, whereas on the scale of individual dendrites or the entire tree, synaptic inputs exhibit dendritic maps where excitatory synapse function varies smoothly with location on the tree. The development of this organization is supported by inhibitory synapses, which are carefully interleaved with excitatory synapses and can flexibly modulate activity and plasticity of excitatory synapses. Here, we summarize recent experimental and theoretical research on the developmental emergence of this synaptic organization and its impact on neural computations.

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Impact of functional synapse clusters on neuronal response selectivity

Cited by 39 publications

References 78 publications

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Emergence of synaptic organization and computation in dendrites

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