Regulation of circuit organization and function through inhibitory synaptic plasticity

Wu, Yue Kris; Miehl, Christoph; Gjorgjieva, Julijana

doi:10.1016/j.tins.2022.10.006

Cited by 43 publications

(42 citation statements)

References 149 publications

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“…The Tac1 cluster labels non-Martinotti cells that target the dendrites of L4 cells [80,81,82], and the Calb2 and Etv1 clusters correspond to fanning-out Martinotti cells [80,5], consistent with a role of Cbln4 in establishing dendritic synapses. But only a subset of the Myh8 cluster-corresponding to T-shaped Martinotti cells [5]-expressed Cbln4, suggesting diverse mechanisms for dendritic targeting. An interneuron's cell type, the plasticity of their input synapses from PCs, and the PC compartments they target are therefore determined before interneurons are fully embedded within cortical circuits, and before pyramidal neurons develop their characteristic morphology and electrophysiology.…”

Section: Box 2 Genetic Basis Of Short-term Facilitationmentioning

confidence: 82%

“…Clustering revealed that these Cbln4 + neurons correspond to previously identified subtypes. The Tac1 cluster labels non-Martinotti cells that target the dendrites of L4 cells [80, 81, 82], and the Calb2 and Etv1 clusters correspond to fanning-out Martinotti cells [80, 5], consistent with a role of Cbln4 in establishing dendritic synapses. But only a subset of the Myh8 cluster—corresponding to T-shaped Martinotti cells [5]— expressed Cbln4, suggesting diverse mechanisms for dendritic targeting.…”

Section: Developmental Trajectory Of Compartment-specific Inhibitionmentioning

confidence: 99%

“…Cortical inhibitory interneurons are a highly diverse group, differing in their morphology, connectivity, and electrophysiology [1]. Decades of experimental and theoretical work have suggested a role for interneurons in many functions [1, 2, 3], including the regulation of neural activity [4, 5], control of synaptic plasticity [6, 7], increasing temporal precision [8, 9], predictive coding [10, 11], and gain modulation [12, 13]. Many of these functions come down to the control of excitation.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Cortical interneurons: fit for function and fit to function? Evidence from development and evolution

Keijser

Sprekeler

2023

Preprint

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Cortical inhibitory interneurons form a broad spectrum of subtypes. This diversity suggests a division of labour, in which each cell type supports a distinct function. In the present era of optimisation-based algorithms, it is tempting to speculate that these functions were the evolutionary or developmental driving force for the spectrum of interneurons we see in the mature mammalian brain. In this study, we evaluated this hypothesis using the two most common interneuron types, parvalbumin (PV) and somatostatin (SST) expressing cells, as examples. PV and SST interneurons control the activity in the cell bodies and the apical dendrites of excitatory pyramidal cells, respectively. But was this compartment-specific inhibition indeed the function for which PV and SST cells originally evolved? Does the compartmental structure of pyramidal cells shape the diversification of PV and SST interneurons over development? To address these questions, we reviewed and reanalysed publicly available data on the development and evolution of PV and SST interneurons on one hand, and pyramidal cell morphology on the other. These data speak against the idea that the compartment structure of pyramidal cells drove the diversification into PV and SST interneurons. In particular, pyramidal cells mature late, while interneurons are likely committed to a particular fate (PV vs. SST) during early development. Moreover, comparative anatomy and single cell RNA-sequencing data indicate that PV and SST cells, but not the compartment structure of pyramidal cells, existed in the last common ancestor of mammals and reptiles. Specifically, turtle and songbird SST cells also express genes that are thought to play a role in compartment-specific inhibition in mammals. PV and SST cells therefore evolved and developed the properties that allow them to provide compartment-specific inhibition before there was selective pressure for this function. This suggests that interneuron diversity originally resulted from a different evolutionary driving force and was only later co-opted for the compartment-specific inhibition it seems to serve in mammals today.

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Section: Box 2 Genetic Basis Of Short-term Facilitationmentioning

confidence: 82%

Section: Developmental Trajectory Of Compartment-specific Inhibitionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cortical interneurons: fit for function and fit to function? Evidence from development and evolution

Keijser

Sprekeler

2023

Preprint

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“…In this view, inhibitory synapse loss may not serve a homeostatic role and may promote cross-modal plasticity by increasing the temporal window of synaptic activity during each calcium transient. Since dendritic disinhibition promotes learning-associated plasticity (Letzkus, Wolff and Luthi, 2015; Mohler and Rudolph, 2017; Artinian and Lacaille, 2018; Wu, Miehl and Gjorgjieva, 2022), disrupted inhibitory synapse adaptation may also interfere with learning or cross-modal plasticity in amyloidosis. Though the direction of neural activity and inhibitory synaptic plasticity in both genotypes are consistent, it is challenging to extrapolate the small effect size of structural synaptic changes to neural and microcircuit activity.…”

Section: Discussionmentioning

confidence: 99%

Amyloid pathology impairs experience-dependent inhibitory synaptic plasticity

Niraula

Yan

Subramanian

2023

Preprint

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Alzheimer's disease is associated with altered neuronal activity, presumably due to impairments in homeostatic synaptic plasticity. Neuronal hyper and hypoactivity are also observed in mouse models of amyloid pathology. Using multicolor two-photon microscopy, we test how amyloid pathology alters the structural dynamics of excitatory and inhibitory synapses and their homeostatic adaptation to altered experience-evoked activity in vivo in a mouse model. The baseline dynamics of mature excitatory synapses and their adaptation to visual deprivation are not altered in amyloidosis. Likewise, the baseline dynamics of inhibitory synapses are not affected. In contrast, despite unaltered neuronal activity patterns, amyloid pathology leads to a selective disruption of homeostatic structural disinhibition on the dendritic shaft. We show that excitatory and inhibitory synapse loss is locally clustered under the nonpathological state, but amyloid pathology disrupts it, indicating impaired communication of changes in excitability to inhibitory synapses.

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“…Although it is still unclear how E/I co-tuning emerges, the dominant view is that it arises via the interaction of several synaptic plasticity mechanisms [19], a hypothesis that has been reinforced by the findings of multiple theoretical studies over the last decade. First, it has been demonstrated that different inhibitory plasticity rules can match static excitatory connectivity [20][21][22][23].…”

Section: Introductionmentioning

confidence: 99%

Structural influences on synaptic plasticity: the role of presynaptic connectivity in the emergence of E/I co-tuning

Giannakakis

Vinogradov

Buendía

et al. 2023

Preprint

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Experimental studies have shown that in cortical neurons, excitatory and inhibitory incoming currents are strongly correlated, which is hypothesized to be essential for efficient computations. Additionally, cortical neurons exhibit strong preference to particular stimuli, which combined with the co-variability of excitatory and inhibitory inputs indicates a detailed co-tuning of the corresponding populations. Such co-tuning is hypothesized to emerge during development in a self-organized manner. Indeed, theoretical studies have demonstrated that a combination of plasticity rules could lead to the emergence of E/I co-tuning in neurons driven by low noise signals from feedforward connections. However, cortical signals are very noisy and originate in highly recurrent networks, which raises a question on the ability of known plasticity mechanisms to self-organize co-tuned connectivity. We demonstrate that high noise levels combined with random recurrence destroy co-tuning. However, we demonstrate that introducing structure in the connectivity patterns of the recurrent E/ I network, the recurrence does not hinder but enhances the formation of the co-tuned selectivity. We employ a combination of analytical methods and simulation-based inference to uncover constraints on the recurrent connectivity that allow E/I co-tuning to emerge. We find that stronger excitatory connectivity within similarly tuned neurons, combined with more homogeneous inhibitory connectivity enhances the ability of plasticity to produce co-tuning in an upstream population. Our results suggest that structured recurrent connectivity controls information propagation and can enhance the ability of synaptic plasticity to learn input-output relationships in higher brain areas.

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Regulation of circuit organization and function through inhibitory synaptic plasticity

Cited by 43 publications

References 149 publications

Cortical interneurons: fit for function and fit to function? Evidence from development and evolution

Cortical interneurons: fit for function and fit to function? Evidence from development and evolution

Amyloid pathology impairs experience-dependent inhibitory synaptic plasticity

Structural influences on synaptic plasticity: the role of presynaptic connectivity in the emergence of E/I co-tuning

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