Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex

Hoehne, Andreas; McFadden, Maureen H; DiGregorio, David A.

doi:10.7554/elife.57344

Cited by 18 publications

(18 citation statements)

References 59 publications

(125 reference statements)

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“…In canonical feedforward circuits, coupling between inhibitory interneurons impacts integration in principal cells (Pham and Haas, 2019). Recent investigations further show the influence of electrical synapses on temporally precise inhibition in feedforward circuits (Chagnaud et al, 2021;Hoehne et al, 2020). Asymmetry, as it can be applied to electrical synapses in these general motifs may impact the many gap junction coupled feedforward and feedback circuits that embed electrical synapses across the brain.…”

Section: Discussionmentioning

confidence: 99%

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Intrinsic Sources and Functional Impacts of Asymmetry at Electrical Synapses

Haas

2022

eNeuro

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Electrical synapses couple inhibitory neurons across the brain, underlying a variety of functions that are modifiable by activity. Despite recent advances, many functions and contributions of electrical synapses within neural circuitry remain underappreciated. Among these are the sources and impacts of electrical synapse asymmetry. Using multi-compartmental models of neurons coupled through dendritic electrical synapses, we investigated intrinsic factors that contribute to effective synaptic asymmetry and that result in modulation of spike timing and synchrony between coupled cells. We show that electrical synapse location along a dendrite, input resistance, internal dendritic resistance, or directional conduction of the electrical synapse itself each alter asymmetry as measured by coupling between cell somas. Conversely, we note that asymmetrical gap junction conductance can be masked by each of these properties. Furthermore, we show that asymmetry modulates spiking timing and latency of coupled cells by up to tens of milliseconds, depending on direction of conduction or dendritic location of the electrical synapse. Coordination of rhythmic activity between two cells also depends on asymmetry. These simulations illustrate that causes of asymmetry are diverse, may not be apparent in somatic measurements of electrical coupling, influence dendritic processing, and produce a variety of outcomes on spiking and synchrony of coupled cells. Our findings highlight aspects of electrical synapses that should always be included in experimental demonstrations of coupling, and when assembling simulated networks containing electrical synapses. 3 SIGNIFICANCE STATEMENTAsymmetry, or unequal transmission of current between two coupled neurons, is a property of electrical synapses often noted but seldom explored. Here we show that multiple intrinsic factors can either produce, or mask, asymmetry. Spike timing and rhythmic synchrony are both affected by asymmetric connections between neurons. These results highlight important consequences of asymmetry that are likely to be recapitulated within coupled networks throughout the brain.

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Section: Discussionmentioning

confidence: 99%

“…In a toadfish vocal circuit, electrical coupling between feedforward inhibitory neurons enhances synchrony and temporal precision (Chagnaud et al, 2021) and a similar effect occurs for cerebellar basket cells (Alcami, 2018;Hoehne et al, 2020). These are some of the functions that could be altered by asymmetry.…”

Section: Introductionmentioning

confidence: 91%

Intrinsic Sources and Functional Impacts of Asymmetry at Electrical Synapses

Haas

2022

eNeuro

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“…In canonical feedforward circuits, coupling between inhibitory interneurons impacts integration in principal cells (Pham & Haas, 2019). Recent investigations further show the influence of electrical synapses on temporally precise inhibition in feedforward circuits (Chagnaud et al, 2021;Hoehne et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…In a canonical model circuit with feedforward inhibition, electrical synapses enhance subthreshold integration (Pham & Haas, 2019). In a toadfish vocal circuit, electrical coupling between feedforward inhibitory neurons enhances synchrony and temporal precision (Chagnaud et al, 2021) and a similar effect occurs for cerebellar basket cells (Hoehne et al, 2020). However, few models have yet included electrical synapses in morphologically extended cells, let alone asymmetrical synapses.…”

Section: Introductionmentioning

confidence: 99%

Electrical synapse asymmetry results from, and masks, neuronal heterogeneity

2021

Preprint

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Electrical synapses couple inhibitory neurons across the brain, underlying a variety of functions that are modifiable by activity. Despite recent advances, many basic functions and contributions of electrical synapses within neural circuitry remain underappreciated. Among these is the source and impact of electrical synapse asymmetry. Using multi-compartmental models of neurons coupled through dendritic electrical synapses, we investigated intrinsic factors that contribute to synaptic asymmetry and that result in modulation of spike time between coupled cells. We show that electrical synapse location along a dendrite, input resistance, internal dendritic resistance, or directional conduction of the electrical synapse itself each alter asymmetry as measured by coupling between cell somas. Conversely, true synapse asymmetry can be masked by each of these properties. Furthermore, we show that asymmetry alters the spiking timing and latency of coupled cells by up to tens of milliseconds, depending on direction of conduction or dendritic location of the electrical synapse. These simulations illustrate that causes of asymmetry are multifactorial, may not be apparent in somatic measurements of electrical coupling, influence dendritic processing, and produce a variety of outcomes on spike timing of coupled cells. Our findings highlight aspects of electrical synapses that should be considered in experimental demonstrations of coupling, and when assembling networks containing electrical synapses.

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“…All the recordings were made with gap junctions intact, including for membrane time constant measurements. However, their expression in SCs is likely to be lower than their basket cell counterparts ( Hoehne et al, 2020 ; Rieubland et al, 2014 ). Overall, the basic electrotonic machinery to filter synaptic responses is already present as soon as SC precursors reach their final location in the outer third of the molecular layer.…”

Section: Discussionmentioning

confidence: 99%

Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons

Biane¹,

Rückerl

Abrahamsson

et al. 2021

eLife

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Synaptic transmission, connectivity, and dendritic morphology mature in parallel during brain development and are often disrupted in neurodevelopmental disorders. Yet how these changes influence the neuronal computations necessary for normal brain function are not well understood. To identify cellular mechanisms underlying the maturation of synaptic integration in interneurons, we combined patch-clamp recordings of excitatory inputs in mouse cerebellar stellate cells (SCs), three-dimensional reconstruction of SC morphology with excitatory synapse location, and biophysical modeling. We found that postnatal maturation of postsynaptic strength was homogeneously reduced along the somatodendritic axis, but dendritic integration was always sublinear. However, dendritic branching increased without changes in synapse density, leading to a substantial gain in distal inputs. Thus, changes in synapse distribution, rather than dendrite cable properties, are the dominant mechanism underlying the maturation of neuronal computation. These mechanisms favor the emergence of a spatially compartmentalized two-stage integration model promoting location-dependent integration within dendritic subunits.

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Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex

Cited by 18 publications

References 59 publications

Intrinsic Sources and Functional Impacts of Asymmetry at Electrical Synapses

Intrinsic Sources and Functional Impacts of Asymmetry at Electrical Synapses

Electrical synapse asymmetry results from, and masks, neuronal heterogeneity

Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons

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