Voltage compartmentalization in dendritic spines in vivo

Cornejo, Víctor Hugo; Ofer, Netanel; Yuste, Rafael

doi:10.1126/science.abg0501

Cited by 86 publications

(80 citation statements)

References 59 publications

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“…Voltage imaging is promising to monitor electrical signals in the developing neocortex in vivo or in utero . Recently, the performance of genetically encoded voltage indicators (GEVIs) has been improved ( Gong et al, 2015 ; Kannan et al, 2018 ; Adam et al, 2019 ; Bando et al, 2019a , b ; Piatkevich et al, 2019 ; Villette et al, 2019 ; Cornejo et al, 2022 ). In contrast with chemical voltage-sensitive dyes (VSDs), GEVIs can be expressed in a cell-type-specific manner, resulting in an improved signal-to-noise ratio.…”

Section: Discussionmentioning

confidence: 99%

Orchestration of Ion Channels and Transporters in Neocortical Development and Neurological Disorders

et al. 2022

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Electrical activity plays crucial roles in neural circuit formation and remodeling. During neocortical development, neurons are generated in the ventricular zone, migrate to their correct position, elongate dendrites and axons, and form synapses. In this review, we summarize the functions of ion channels and transporters in neocortical development. Next, we discuss links between neurological disorders caused by dysfunction of ion channels (channelopathies) and neocortical development. Finally, we introduce emerging optical techniques with potential applications in physiological studies of neocortical development and the pathophysiology of channelopathies.

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Section: Discussionmentioning

confidence: 99%

Orchestration of Ion Channels and Transporters in Neocortical Development and Neurological Disorders

et al. 2022

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“…It follows that our results call into question several existing hypotheses on the electrical role of spines. For example, it has been postulated that spines may initiate APs (Araya et al, 2006b), that spines cause the reduction of location-dependent variability of local EPSP amplitude and normalize synaptic activation of NMDA receptors and voltage-gated channels (Gulledge et al, 2012), that spines amplify EPSPs up to 45-fold thus facilitating electrical interactions among coactive inputs and promoting associated forms of plasticity and storage (Harnett et al, 2012), that spine necks severely attenuate EPSP signals (Kwon et al, 2017), that spine geometry plays a key role in shaping the EPSP time course (Lagache et al, 2019), that spines are elementary voltage compartments that could be important for dendritic integration and disease states (Cornejo et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…The accuracy of calibration of profoundly distorted optical signals based on modeling is uncertain. Another recent effort to define the electrical role of spines in vivo (Cornejo et al, 2022) used two-photon microscopy and a genetically encoded protein voltage sensor to monitor electrical events in spines and dendrites during spontaneous activity and sensory stimulation. This approach is an impressive example of integrating several cutting-edge experimental techniques.…”

Section: Discussionmentioning

confidence: 99%

“…Another group of studies postulate high R neck based on indirect measurements that are difficult to interpret unambiguously (Bloodgood and Sabatini, 2005; Araya et al, 2006a, 2006b, 2014; Grunditz et al, 2008; Bloodgood et al, 2009; Harnett et al, 2012; Tønnesen et al, 2014; Bywalez et al, 2015; Acker et al, 2016; Hage et al, 2016; Beaulieu-Laroche and Harnett, 2018). A third group of studies postulate high R neck based on the results from electrical and optical recordings that require extensive corrections (Jayant et al, 2016; Kwon et al, 2017; Cartailler et al, 2018; Cornejo et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Contribution of individual excitatory synapses on dendritic spines to electrical signalling

Weng

Ceballos

Zečević

2022

Preprint

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Even though dendritic spines are widely considered the elementary computational units of the brain, the current understanding of the exact contribution of individual synapses on spines to the electrical signaling in neurons is incomplete. We combined the techniques of whole-cell recording and voltage imaging to monitor directly unitary excitatory postsynaptic potentials evoked by two-photon glutamate uncaging (uEPSPs) on individual dendritic spines. We analyzed the initiation, temporal summation, and propagation of uEPSPs from the spine head to the parent dendrite and to the cell body in neocortical pyramidal neurons. Our measurements show no significant attenuation of uEPSPs across the spine neck in different types of pyramidal neurons. This result implies that spine synapses are not electrically isolated from parent dendrites and that spines do not serve a meaningful electrical role. Using the same techniques, we next characterized temporal summation of uEPSPs induced at individual spine synapses by repetitive glutamate uncaging mimicking burst activity of presynaptic neurons. We found that pharmacological block of desensitization of AMPA receptors increased the amplitude of cumulative uEPSP response in the spines head and, consequently, in parent dendrite and soma. Thus, responses to high frequency repetitive quantal EPSPs are strictly limited in amplitude and waveform by AMPA receptor desensitization at the site of origin thereby preventing synaptic saturation.

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“…However, as suggested by experimental findings [Cornejo et al, 2021], the actual value of the somatic membrane potential is hidden from the synapse and therefore the synapse has to infer the value of u from the sparse information that propagates back from the soma into the dendrites. We consider that this sparse feedback is implemented by bAP events z, given by the firing times t…”

Section: A Synaptic Account Of the Free Energy Principlementioning

confidence: 99%

Synapses learn to utilize pre-synaptic noise for the prediction of postsynaptic dynamics

Kappel

Tetzlaff

2022

Preprint

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Synapses in the brain are highly noisy, which leads to a large trial-by-trial variability. Given how costly synapses are in terms of energy consumption these high levels of noise are surprising. Here we propose that synapses use their noise to represent uncertainties about the activity of the post-synaptic neuron. To show this we utilize the free-energy principle (FEP), a well-established theoretical framework to describe the ability of organisms to self-organize and survive in uncertain environments. This principle provides insights on multiple scales, from high-level behavioral functions such as attention or foraging, to the dynamics of single microcircuits in the brain, suggesting that the FEP can be used to describe all levels of brain function. The synapse-centric account of the FEP that is pursued here, suggests that synapses form an internal model of the somatic membrane dynamics, being updated by a synaptic learning rule that resembles experimentally well-established LTP/LTD mechanisms. This approach entails that a synapse utilizes noisy processes like stochastic synaptic release to also encode its uncertainty about the state of the somatic potential. Although each synapse strives for predicting the somatic dynamics of its neuron, we show that the emergent dynamics of many synapses in a neuronal network resolve different learning problems such as pattern classification or closed-loop control in a dynamic environment. Hereby, synapses coordinate their noise processes to represent and utilize uncertainties on the network level in behaviorally ambiguous situations.

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Voltage compartmentalization in dendritic spines in vivo

Cited by 86 publications

References 59 publications

Orchestration of Ion Channels and Transporters in Neocortical Development and Neurological Disorders

Orchestration of Ion Channels and Transporters in Neocortical Development and Neurological Disorders

Contribution of individual excitatory synapses on dendritic spines to electrical signalling

Synapses learn to utilize pre-synaptic noise for the prediction of postsynaptic dynamics

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