Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity
- Department of Neurosciences, Katholieke Universiteit Leuven, Belgium
- Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, United States
- Department of Neuroscience, University of Texas at Austin, United States
- Department of Mathematics and Statistics, Swarthmore College, United States
- Department of Neuroscience, University of Wisconsin-Madison, United States
Figures
Figure 1 with 5 supplements
Sharp ITD-sensitivity to clicks in LSO but not MSO.
(A) Click-ITD function (10 repetitions) of an LSO principal cell (CF = 5.7 kHz). Data are represented as mean ± SEM. Red circles indicate ITD values near the trough when the spike rate reached 20% …
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Figure 1—source data 1
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Figure 1—figure supplement 1
Physiological data of LSO cells in Figure 1.
(A) Top: IID function to 5.7 kHz tones for the same principal LSO neuron as in Figure 1A. Data are represented as mean ± SEM. Ipsilateral sound level was kept constant at 60 dB SPL. Stimulus …
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Figure 1—figure supplement 1—source data 1
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Figure 1—figure supplement 2
Population data of ITD functions of Figure 1G–I, without centering the left flank of the central trough (LSO) or peak (MSO) at 0 ms.
Numerical data represented as graphs in this figure are available in a source data file (Figure 1—figure supplement 2—source data 2).
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Figure 1—figure supplement 2—source data 2
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Figure 1—figure supplement 3
ITD-sensitivity to clicks at different sound levels.
(A,B) For two principal LSO neurons, click ITD functions at different monaural sound levels are shown (IID = 0). Higher sound levels result in steeper slopes and narrower halfwidths. (A) BF = 437 Hz;…
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Figure 1—figure supplement 3—source data 3
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Figure 1—figure supplement 4
ITD-sensitivity to clicks is steeper than to sustained sounds for LSO cells.
(A) ITD functions to noise (blue) and clicks (black) for 8 LSO neurons. Noise ITD functions include all spikes beyond 10 ms after stimulus onset. Top row are data from juxtacellular recordings, …
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Figure 1—figure supplement 4—source data 4
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Figure 1—figure supplement 5
Steep ITD-sensitivity to transients extends to rustling stimuli.
(A) Bottom panel: waterfall plot of responses to a rustling stimulus, an irregular succession of transients designed to mimic natural sounds such as crumpling of leaves (Ewert et al., 2012), from a …
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Figure 1—figure supplement 5—source data 5
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Figure 2 with 1 supplement
Precise timing and interaction of IPSPs and EPSPs in LSO neurons.
(A–B) Example responses to ipsilateral clicks (top panels) and contralateral clicks (bottom panels) for a principal LSO cell (A; CF = 12 kHz; 50 dB SPL; 10 repetitions) and a non-principal LSO cell …
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Figure 2—source data 1
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Figure 2—figure supplement 1
Precise interaction of IPSPs and EPSPs for another principal LSO neuron.
(A–C) Similar to Figure 2D–F, for another principal LSO neuron (CF = 7.5 kHz). Numerical data represented as graphs in this figure are available in a source data file (Figure 2—figure supplement …
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Figure 2—figure supplement 1—source data 1
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Figure 4 with 1 supplement
In vitro recordings reveal powerful inhibition for synaptically evoked but not for simulated IPSPs.
(A) Voltage responses from a principal LSO neuron recorded in a brain slice, for which the ipsilateral inputs were activated by electric shocks and the contralateral input was simulated by …
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Figure 4—source data 1
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Figure 4—figure supplement 1
In vitro recordings reveal powerful inhibition for synaptically evoked IPSPs but not for IPSPs simulated by current injection.
(A–B) Similar to Figure 4A and B, but now inhibitory (A) or excitatory (B) synaptic inputs were simulated by injecting currents instead of conductances by dynamic clamp. This experiment was done in …
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Figure 4—figure supplement 1—source data 1
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Figure 5
Glycinergic innervation of the axon initial segment of LSO neurons.
(A) An example of an LSO in a coronal tissue section from the Mongolian gerbil outlining subregions targeted for SR-SIM microscopy labeled with gephyrin (red), ankyrinG (cyan), and DAPI (blue). All …
Figure 6 with 1 supplement
Electron microscopy reveals synaptic terminals on an LSO principal cell’s axon initial segment.
(A) Camera lucida drawing of an LSO principal cell that was intracellularly recorded from and labeled, in vivo. This cell corresponds to cell two in Franken et al., 2018, their Figure 2A. Arrows …
Figure 6—figure supplement 1
Electron microscopy reveals synaptic terminals on the axon initial segment of principal LSO cells but not of principal MSO cells.
(A) Right: camera lucida drawing of an LSO principal cell that was intracellularly recorded from and labeled in vivo, and its location in a coronal section of the LSO. Numbers and arrows point to …
Figure 7 with 2 supplements
ITD-tuning in a two-compartment LSO neuron model.
(A) ITD-tuning is substantially deeper when inhibitory inputs target AIS as compared to the same total number of inputs targeting the soma only. (B) Soma voltage showing detailed timing of responses …
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Figure 7—source data 1
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Figure 7—figure supplement 1
Two-compartment LSO neuron model.
(A–E) Model parameters depend on coupling constants. Each coupling constant pair () defines a model with soma voltage dynamics constructed to match known properties of LSO neurons. (F) AIS input …
Figure 7—figure supplement 2
ITD tuning in two-compartment LSO neuron model with synaptic kinetics adapted from Beiderbeck et al., 2018.
See Materials and methods for details. Figure layout same as Figure 7. Numerical data represented as graphs in this figure are available in a source data file (Figure 7—figure supplement 2—source …
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Figure 7—figure supplement 2—source data 1
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Figure 8 with 2 supplements
LSO neurons show graded latency-intensity changes which disambiguate spatial tuning.
(A) Cartoon showing change in spike probability for changing IID. Yellow area shows approximate region of physiological IID values. Traces below each plot represent the timing and amplitude of ipsi- …
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Figure 8—source data 1
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Figure 8—figure supplement 1
Individual traces corresponding to the mean data shown in Figure 8D and E.
(A) Same cell as Figure 8D. Top panel shows responses to ipsilateral clicks, bottom panel to contralateral clicks. Traces are color-coded according to SPL (same color legend in A and B). SPL is …
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Figure 8—figure supplement 1—source data 1
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Figure 8—figure supplement 2
Similar as Figure 8K and L, for three additional LSO neurons.
(A–C) Similar response maps to combined ITD and IID variations as Figure 8K and L, for (A) a non-principal (type 5) LSO cell (CF = 2.0 kHz), (B) another principal LSO cell (CF = 12 kHz) and (C) a …
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Figure 8—figure supplement 2—source data 2
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Figure 3 with 1 supplement
Weak ITD-tuning in MSO neurons results from a breakdown of coincidence detection for transients.
(A) Top panel: Example responses to ipsilateral clicks (top panel) and contralateral clicks (bottom panel) for an MSO cell (CF = 1.8 kHz). Sound level 70 dB SPL. 30 repetitions shown. (B) Similar to …
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Figure 3—source data 1
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Figure 3—figure supplement 1
Monaural stimulation often leads to double events both in LSO and MSO.
In both LSO and MSO, double events in response to a single monaural click were sometimes observed, for both ipsi- and contralateral stimulation. Each pair of panels shows individual responses to …
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Figure 3—figure supplement 1—source data 1
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Author response image 1
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Strain, strain background (Meriones unguiculatus, male and female) | Wildtype | In vivo: Janvier Labs In vitro: Animals raised in colony at at UT-Austin Animal Resource Center (breeders obtained from Charles River Laboratories) | ||
| Antibody | Anti-Synaptophysin1 (Guinea pig polyclonal) | Synaptic Systems | Cat# 101–004; RRID:AB_1210382 | (1:500) |
| Antibody | Anti-AnkyrinG (rabbit polyclonal) | Galiano et al., 2012 | (1:200) Courtesy of Dr. Matthew Rasband (Baylor College of Medicine) | |
| Antibody | Anti-Gephyrin (mouse monoclonal) | Synaptic Systems | Cat# 147–011; RRID:AB_887717 | (1:200) |
| Software, algorithm | MATLAB | The Mathworks | ||
| Software, algorithm | IGOR-Pro | Wavemetrics | ||
| Software, algorithm | MafDC | Yang et al., 2015 | Courtesy of Dr. Matthew Xu-Friedman | |
| Software, algorithm | SIM-post processing software | Zeiss | ||
| Software, algorithm | Metamorph | Molecular Devices |
Additional files
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Source code 1
Code to generate figures of the computational model.
- https://cdn.elifesciences.org/articles/62183/elife-62183-code1-v2.zip
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Transparent reporting form
- https://cdn.elifesciences.org/articles/62183/elife-62183-transrepform-v2.pdf
