Dynamic Tuning of Electrical and Chemical Synaptic Transmission in a Network of Motion Coding Retinal Neurons

Trenholm, Stuart; McLaughlin, Amanda J.; Schwab, David J.; Awatramani, Gautam B.

doi:10.1523/jneurosci.0808-13.2013

Cited by 49 publications

(59 citation statements)

References 60 publications

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“…4B). Differentiation of the spikelet waveform generated a waveform similar to the cell-attached spike waveform (data not shown; Trenholm et al 2013), and the peak of the cell-attached spike preceded the peak of the differentiated spikelet by 0.3 Ϯ 0.2 ms, similar to the spike-to-spikelet latency observed in paired whole cell Golgi cell recordings. The latency to the first cell-attached spike from the beginning of the step in the Golgi cell decreased as a function of voltage, and the frequency of Golgi cell APs increased as a function of voltage (Fig.…”

Section: Cx36supporting

confidence: 59%

“…The DJP of the spikelet is too weak (Յ1 mV) to directly evoke spikes in postjunctional cells at typical resting membrane potentials (Trenholm et al 2013) and is so brief (half-width of ϳ3 ms) that coupled Golgi cells would need to be close to threshold at the same time in order to take advantage of the DJP. The HJP is considerably longer than the DJP (half-width ϳ80 ms) and thus could act on longer timescales than the DJP to inhibit firing of coupled Golgi cells.…”

Section: Sources Of Chemical Inhibitory Input To Cochlear Nucleusmentioning

confidence: 99%

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Auditory Golgi cells are interconnected predominantly by electrical synapses

Yaeger

Trussell

2016

Journal of Neurophysiology

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Section: Cx36supporting

confidence: 59%

Section: Sources Of Chemical Inhibitory Input To Cochlear Nucleusmentioning

confidence: 99%

Auditory Golgi cells are interconnected predominantly by electrical synapses

Yaeger

Trussell

2016

Journal of Neurophysiology

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“…Near eye-opening, there is robust gap junction coupling among different DSGC subtypes [37], while in adult, only the superior-preferring DSGC subtype is coupled [38][39][40] Hence, each DSGC may be tuned to a cardinal axis, but input via a gap junction from a DSGC tuned to a different cardinal direction may cause the final tuning of the DSGC to lie off its cardinal axis. Previous studies indicate that darkrearing delayed the decoupling process but did not prevent it.…”

Section: Potential Activity-dependent Mechanismsmentioning

confidence: 99%

Role for Visual Experience in the Development of Direction-Selective Circuits

Bos¹,

Gainer²,

Feller³

2017

Current Biology

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SUMMARYVisually-guided behavior can depend critically on detecting the direction of object movement. This computation is first performed in the retina where direction is encoded by direction-selective ganglion cells (DSGCs) that respond strongly to an object moving in the preferred direction and weakly to an object moving in the opposite, or null, direction (reviewed in [1]). These DSGCs come in multiple types that are classified based on their morphologies, response properties and targets in the brain. This study focuses on two types -ON and ON-OFF DSGCs. Though animals can sense motion in all directions, the preferred directions of DSGCs in adult retina cluster along distinct directions that we refer to as the cardinal axes. ON DSGCs have three cardinal axestemporal, ventral and dorsonasal -while ON-OFF DSGCs have four -nasal, temporal, dorsal, and ventral. How these preferred directions emerge during development is still not understood. Several studies have demonstrated that ON [2] and ON-OFF DSGCs are well tuned at eye-opening, and even a few days prior to eye-opening, in rabbits [3], rats [4] and mice [5][6][7][8], suggesting that visual experience is not required to produce direction selective tuning. However, here we show that at eye-opening the preferred directions of both ON and ON-OFF DSGCs are diffusely distributed and that visual deprivation prevents the preferred directions from clustering along the cardinal axes. Our findings indicate a critical role for visual experience in shaping responses in the retina. HHS Public Access RESULTS Clustering of DSGC preferred directions along cardinal axes after eye-opening requires visual experienceWe used two-photon calcium imaging to study the development of DSGC populations in mouse retina. This imaging technique has proven to be quite powerful in characterizing the receptive field properties of retinal ganglion cells [9][10][11][12]. We loaded retinas of WT mice near eye-opening (P13-P14) and in adulthood (>P30) with the calcium dye Oregon green 488 BAPTA-1 hexapotassium salt (OGB-1) via electroporation, thus uniformly labeling the ganglion cell layer ( Figure 1A; see Supplemental Information). Ventral portions of the retina were stimulated with light centered at 385 nm to maximally activate UV-cones [13,14] while minimizing cross talk with the imaging detectors ( Figure S1). This approach allowed us to record from all DSGC subtypes within a single field of view (~40000 μm 2 ).To identify DSGCs, we first used full field UV-light flashes to classify cells as ON, OFF or ON-OFF retinal ganglion cells (RGCs) ( Figure S1; Table S1). We found that around 80% of the cells in the ganglion cell layer of young and adult retinas responded to light flashes with changes in fluorescence (Table S1), similar to the RGC percentages reported in previous studies [9,11,12]. In addition, over development we observed a decrease in the percentage of ON-OFF RGCs (28.03% at P13-14 to 20.84% in adult) (Table S1) [15].Second, we used light bars on a dark background drifting in 8 dir...

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“…Trenholm and colleagues [•31] have found that electrical coupling among the dorsally coding On-Off directionally-selective ganglion cells imparts the remarkable ability to encode the leading edge of a stimulus at the same spatial location regardless of the speed of stimulus motion. This lag normalization depends on the transmission of a subthreshold excitatory receptive field surround through the electrical synapses to reinforce sparse synaptic input from distant stimuli within the classical receptive field center [••32]. This lateral priming does not result in back-propagation of excitation after the trailing edge of the stimulus passes, which would result in stretching of the coded object.…”

Section: Seeing All Of the Lightmentioning

confidence: 99%

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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Dynamic Tuning of Electrical and Chemical Synaptic Transmission in a Network of Motion Coding Retinal Neurons

Cited by 49 publications

References 60 publications

Auditory Golgi cells are interconnected predominantly by electrical synapses

Auditory Golgi cells are interconnected predominantly by electrical synapses

Role for Visual Experience in the Development of Direction-Selective Circuits

The ever-changing electrical synapse

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