The extent and strength of electrical coupling between inferior olivary neurons is heterogeneous

Hoge, Gregory; Davidson, Kimberly G. V.; Yasumura, Thomas; Castillo, Pablo E.; Rash, John E.; Pereda, Alberto E.

doi:10.1152/jn.00789.2010

Cited by 87 publications

(84 citation statements)

References 65 publications

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“…A potentially similar form of long-term depression of electrical synapses has been described in the thalamic reticular nucleus [37]. Coupling among IO neurons has been found to be highly variable [38], and the NMDA receptor-dependent mechanisms described by Mathy et al [••36] and Turecek et al [••10] can explain how local excitatory input can tune coupling strength in a manner analogous to the delicate balance between long-term potentiation and long-term depression in central glutamatergic synapses.…”

Section: Timing Is Everythingmentioning

confidence: 94%

The ever-changing electrical synapse

O’Brien

2014

Current Opinion in Neurobiology

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A wealth of research has revealed that electrical synapses in the central nervous system exhibit a high degree of plasticity. Several recent studies, particularly in the retina and inferior olive, highlight this plasticity. Three classes of mechanisms can alter electrical coupling over time courses ranging from milliseconds to days. Changes of membrane conductance through synaptic input or spiking activity shunt current and decouple neurons on the millisecond time scale. Such activity can also alter coupling symmetry, rectifying electrical synapses. More stable rectification can be accomplished through molecular asymmetry of the synapse itself. On the minutes time scale, changes in connexin phosphorylation can change coupling quasi-stably with order of magnitude dynamic range. On the hours to days time scale, changes in expression level of connexins alter coupling through the course of circadian time, over developmental time, or in response to tissue injury. Combined, all of these mechanisms allow electrical coupling to be highly dynamic, changing in response to demands at the whole network level, in small portions of a network, or at the level of an individual synapse.

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Section: Timing Is Everythingmentioning

confidence: 94%

The ever-changing electrical synapse

O’Brien

2014

Current Opinion in Neurobiology

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“…6), paired recordings coupled with anatomical descriptions (7), and frequency-dependent impedance measurements (8). The first two methods do not readily distinguish direct connections from indirect connections involving an intermediate IN (7,9,10), and all three methods are labor intensive and difficult to implement in a fully quantitative manner. In addition, they do not provide information on the spatial arrangement of the GJs.…”

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confidence: 99%

Estimating functional connectivity in an electrically coupled interneuron network

Alcamí

Marty

2013

Proc. Natl. Acad. Sci. U.S.A.

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Even though it has been known for some time that in many mammalian brain areas interneurons are electrically coupled, a quantitative description of the network electrical connectivity and its impact on cellular passive properties is still lacking. Approaches used so far to solve this problem are limited because they do not readily distinguish junctions among direct neighbors from indirect junctions involving intermediary, multiply connected cells. In the cerebellar cortex, anatomical and functional evidence indicates electrical coupling between molecular layer interneurons (basket and stellate cells). An analysis of the capacitive currents obtained under voltage clamp in molecular layer interneurons of juvenile rats or mice reveals an exponential component with a time constant of ∼20 ms, which represents capacitive loading of neighboring cells through gap junctions. These results, taken together with dual cell recording of electrical synapses, have led us to estimate the number of direct neighbors to be ∼4 for rat basket cells and ∼1 for rat stellate cells. The weighted number of neighbors (number of neighbors, both direct and indirect, weighted with the percentage of voltage deflection at steady state) was 1.69 in basket cells and 0.23 in stellate cells. The last numbers indicate the spread of potential changes in the network and serve to estimate the contribution of gap junctions to cellular input conductance. In conclusion the present work offers effective tools to analyze the connectivity of electrically connected interneuron networks, and it indicates that in juvenile rodents, electrical communication is stronger among basket cells than among stellate cells. To model the functional role of gap junctions (GJs) in the IN network and in cellular computation, it is necessary to determine the number of cells that are connected to a given cell, as well as the geometry of the network. Methods that have been developed to extract this information include dye coupling analysis (e.g., ref. 6), paired recordings coupled with anatomical descriptions (7), and frequency-dependent impedance measurements (8). The first two methods do not readily distinguish direct connections from indirect connections involving an intermediate IN (7,9,10), and all three methods are labor intensive and difficult to implement in a fully quantitative manner. In addition, they do not provide information on the spatial arrangement of the GJs. Therefore, the data that have been exploited for modeling GJ connectivity in IN networks are missing critical elements.In the cerebellum, Golgi cells and molecular layer interneurons (MLIs) have been shown to form anatomical and functional networks involving GJs that are specific to a given cell type (6,(11)(12)(13)(14). In both cases GJs may be involved in the generation of concerted oscillations under some pharmacological conditions (12, 15), and spikelets (spikes of coupled cells filtered through GJs) have been shown to encode sensory information in MLIs (16). MLIs are particularly interesting because th...

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“…However, the coupling shows a striking level of heterogeneity, which may serve to finely influence the synchronization of IO neurons (Hoge et al 2010). This raises the possibility that variations in coupling could result from glomerulus-specific long-term modulation of gap junctions.…”

Section: Ultrastructure Of the Inferior Olivary Neuropil Glomeruli Anmentioning

confidence: 99%

Inferior Olive: All Ins and Outs

Gruijl

Bosman

Zeeuw

et al. 2013

Handbook of the Cerebellum and Cerebellar Disorders

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The inferior olive provides all climbing fibers to the Purkinje cells in the cerebellar cortex and thereby has a strong impact on cerebellar output. As a consequence, the integration of inputs to olivary neurons as well as their intrinsic properties are critical for cerebellar function. In this chapter, all issues that are relevant for their ultimate function are addressed. This chapter starts by reviewing developmental aspects such as the origin and migratory routes of inferior olivary neurons and a description of their axonal outgrowth into climbing fibers innervating Purkinje cells. Subsequently, a detailed description of the olivary subdivisions and the ultrastructure of their neuropil is provided. This is characterized by the presence of dendro-dendritic gap junctions located in glomeruli and by the consistently combined excitatory and inhibitory innervation of their coupled spines. Furthermore, the electrophysiological behavior of olivary neurons is described and discussed. Finally, these unique properties are integrated in cellular and system models. Both type of models show that the inferior olive is very well able to control both rate

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The extent and strength of electrical coupling between inferior olivary neurons is heterogeneous

Cited by 87 publications

References 65 publications

The ever-changing electrical synapse

The ever-changing electrical synapse

Estimating functional connectivity in an electrically coupled interneuron network

Inferior Olive: All Ins and Outs

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