Functional Convergence at the Retinogeniculate Synapse

Litvina, Elizabeth Y.; Chen, Chinfei

doi:10.1016/j.neuron.2017.09.037

Cited by 96 publications

(86 citation statements)

References 47 publications

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“…This revealed a striking, ß30-fold difference in the unitary synaptic conductances between inhibition and excitation converging onto LSO neurons, at least when excitation and inhibition are both measured under conditions of high driving forces (ß70 mV). The minimal optogenetic stimulation method used here might also be useful for measuring the strength of unitary synaptic events in other circuits (see also Lu & Trussell, 2016;Litvina & Chen, 2017).…”

Section: Strong But Variable Unitary Inhibition Onto Lso Neuronsmentioning

confidence: 99%

Specific synaptic input strengths determine the computational properties of excitation–inhibition integration in a sound localization circuit

Gjoni

Zenke

Bouhours

et al. 2018

The Journal of Physiology

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The lateral superior olive (LSO) is a binaural nucleus in the auditory brainstem in which excitation from the ipsilateral ear is integrated with inhibition from the contralateral ear. It is unknown whether the strength of the unitary inhibitory and excitatory inputs is adapted to allow for optimal tuning curves of LSO neuron action potential (AP) firing. Using electrical and optogenetic stimulation of afferent synapses, we found that the strength of unitary inhibitory inputs to a given LSO neuron can vary over a ∼10-fold range, follows a roughly log-normal distribution, and, on average, causes a large conductance (9 nS). Conversely, unitary excitatory inputs, stimulated optogenetically under the bushy-cell specific promoter Math5, were numerous, and each caused a small conductance change (0.7 nS). Approximately five to seven bushy cell inputs had to be active simultaneously to bring an LSO neuron to fire. In double stimulation experiments, the effective inhibition window caused by IPSPs was short (1-3 ms) and its length depended on the inhibitory conductance; an ∼2-fold stronger inhibition than excitation was needed to suppress AP firing. Computational modelling suggests that few, but strong, unitary IPSPs create a tuning curve of LSO neuron firing with an appropriate slope and midpoint. Furthermore, weak but numerous excitatory inputs reduce the spontaneous AP firing that LSO neurons would otherwise inherit from their upstream auditory neurons. Thus, the specific connectivity and strength of unitary excitatory and inhibitory inputs to LSO neurons is optimized for the computations performed by these binaural neurons.

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Section: Strong But Variable Unitary Inhibition Onto Lso Neuronsmentioning

confidence: 99%

Specific synaptic input strengths determine the computational properties of excitation–inhibition integration in a sound localization circuit

Gjoni

Zenke

Bouhours

et al. 2018

The Journal of Physiology

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“…Thus, we cannot safely conclude on the number of inhibitory inputs received by a single LSO neuron based on the present SBEM data. A similar disagreement between the number of optogenetically stimulated synaptic inputs, and the number of inputs found in connectomics studies on the light and electron microscopic level (Morgan et al 2016;Rompani et al 2017), has recently been found at the retinogeniculate synapse (Litvina & Chen, 2017).…”

Section: Technical Considerationsmentioning

confidence: 55%

Ultrastructural basis of strong unitary inhibition in a binaural neuron

Gjoni

Aguet

Sahlender

et al. 2018

The Journal of Physiology

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Binaural neurons in the lateral superior olive (LSO) integrate sound information arriving from each ear, and powerful glycinergic inhibition of these neurons plays an important role in this process. In the present study, we investigated the ultrastructural basis for strong inhibitory inputs onto LSO neurons using serial block face scanning electron microscopy. We reconstructed axon segments that make contact with the partially reconstructed soma and proximal dendrite of a mouse LSO neuron at postnatal day 18. Using functional measurements and the Sr method, we find a constant quantal size but a variable quantal content between 'weak' and 'strong' unitary IPSCs. A 3-D reconstruction of a LSO neuron and its somatic synaptic afferents reveals how a large number of inhibitory axons intermingle in a complex fashion on the soma and proximal dendrite of an LSO neuron; a smaller number of excitatory axons was also observed. A given inhibitory axon typically contacts an LSO neuron via several large varicosities (average diameter 3.7 μm), which contain several active zones (range 1-11). The number of active zones across individual axon segments was highly variable. These data suggest that the variable unitary IPSC amplitude is caused by a variable number of active zones between inhibitory axons that innervate a given LSO neuron. The results of the present study show that relatively large multi-active zone varicosities, which can be repeated many times in a given presynaptic axon, provide the ultrastructural basis for the strong multiquantal inhibition received by LSO neurons.

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“…Interestingly, using ontogenetic stimulation of retinal terminals expressing channelrhodopsin (ChR2) Litvina and Chen (Litvina and Chen, 2017) have recently confirmed a higher level functional retinal convergence onto dLGN relay cells. Here, we sought to understand the molecular mechanisms underlying this newly appreciated convergence in visual thalamus.…”

Section: Disscussionmentioning

confidence: 96%

LRRTM1 underlies synaptic convergence in visual thalamus

Monavarfeshani

Stanton

Name

et al. 2017

Preprint

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It has long been thought that the mammalian visual system is organized into parallel pathways, with incoming visual signals being parsed in the retina based on feature (e.g. color, contrast and motion) and then transmitted to the brain in unmixed, feature-specific channels. To faithfully convey feature-specific information from retina to cortex, thalamic relay cells must receive inputs from only a small number of functionally similar retinal ganglion cells. However, recent studies challenged this by revealing substantial levels of retinal convergence onto relay cells. Here, we sought to identify mechanisms responsible for the assembly of such convergence. Using an unbiased transcriptomics approach and targeted mutant mice, we discovered a critical role for the synaptic adhesion molecule Leucine Rich Repeat Transmembrane Neuronal 1 (LRRTM1) in the emergence of retinothalamic convergence. Importantly, LRRTM1 mutant mice display impairment in visual behaviors, suggesting a functional role of retinothalamic convergence in vision.

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Functional Convergence at the Retinogeniculate Synapse

Cited by 96 publications

References 47 publications

Specific synaptic input strengths determine the computational properties of excitation–inhibition integration in a sound localization circuit

Specific synaptic input strengths determine the computational properties of excitation–inhibition integration in a sound localization circuit

Ultrastructural basis of strong unitary inhibition in a binaural neuron

LRRTM1 underlies synaptic convergence in visual thalamus

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