Retinal input integration in excitatory and inhibitory neurons in the mouse superior colliculus in vivo

  1. Carolin Gehr
  2. Jeremie Sibille
  3. Jens Kremkow  Is a corresponding author
  1. Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Germany
  2. Bernstein Center for Computational Neuroscience Berlin, Germany
  3. Institute for Theoretical Biology, Humboldt-Universität zu Berlin, Germany
  4. Einstein Center for Neurosciences Berlin, Germany
13 figures and 1 additional file

Figures

Figure 1 with 2 supplements
Simultaneous extracellular recordings of retinal ganglion cell (RGC) axons and superior colliculus (SC) neurons combined with optotagging identifies GABAergic neurons in VGAT-ChR2 mice.

(A) Recording configuration for tangential electrode insertion and optotagging in the visual layers of mouse SC. The optogenetic fiber is inserted perpendicularly to the Neuropixels probe to …

Figure 1—figure supplement 1
Optogenetic response and spatial distribution of excitatory and inhibitory superior colliculus (SC) neurons.

(A) Multi-unit activity in response to optogenetic stimulation (100 or 50 ms) using a square wave pulse or a Gaussian-shaped LED pulse for three individual recordings. (B) Spatial distribution of …

Figure 1—figure supplement 2
Spike waveform features analysis for GABAergic and non-GABAergic neuron populations in the superior colliculus (SC).

(A) Top: Illustration of features extracted from single-channel waveforms (magenta circles indicate the trough and peak). Middle and bottom: Single-channel mean waveforms for non-GABAergic (gray; …

Retinal innervation is similarly strong to excitatory and inhibitory superior colliculus (SC) neurons.

(A) Monosynaptically connected retinal ganglion cell (RGC)-SC excitatory neuron (EXN) (gray) and RGC-SC inhibitory neuron (IN) (blue) pairs are identified via cross-correlogram (CCG) analysis. (B) …

Figure 2—source code 1

Code to plot Figure 2D, F, G.

https://cdn.elifesciences.org/articles/88289/elife-88289-fig2-code1-v1.zip
Figure 2—source data 1

Data for Figure 2D describing the distance between retinal ganglion cell (RGC) axon and superior colliculus (SC) neuron on the electrode probe; and Figure 2F, G efficacy values.

https://cdn.elifesciences.org/articles/88289/elife-88289-fig2-data1-v1.xlsx
Characterization of functional similarity between retinocollicular connected pairs.

(A) Top: Spatiotemporal receptive fields (STRF) evoked by dark (SD) and light (SL) sparse noise stimuli for retinal ganglion cell (RGC)-superior colliculus (SC) excitatory neuron (EXN) and RGC-SC …

Paired-spike dynamics: Second retinal spikes are more efficient in driving superior colliculus (SC) response.

(A) Schematic illustrating the temporal dynamics between two successive retinal ganglion cell (RGC) spikes. Pairs of RGC spikes with a minimum inter-spike interval (ISI) of 5 ms and maximum ISI of …

Figure 4—source code 1

Code to plot Figure 4C–F.

https://cdn.elifesciences.org/articles/88289/elife-88289-fig4-code1-v1.zip
Figure 4—source data 1

Data for Figure 4C: efficacy values in response to first and second retinal ganglion cell (RGC) spikes, Figure 4D, E: paired-spike ratio (PSR) values, and Figure 4F: PSR values for different groups.

https://cdn.elifesciences.org/articles/88289/elife-88289-fig4-data1-v1.xlsx
Figure 5 with 1 supplement
Connection contribution is higher in connected retinal ganglion cell (RGC)-superior colliculus (SC) excitatory neuron (EXN) pairs.

(A) Example cross-correlograms (CCGs) of monosynaptically connected RGC-SC EXN (left) and RGC-SC inhibitory neuron (IN) (right) pairs. Connected pairs were identified by their peaks in the CCGs …

Figure 5—figure supplement 1
Contribution as a function of firing rate during different stimulus conditions.

Relationships between contribution and the conditions during natural movie (NM), phase scrambled movie (PSM), gray background (Bkg), and checkerboard (Chk) for retinal ganglion cell (RGC) superior …

Author response image 1
Efficacy measure of connected RGC-SC pairs as a function of the mean firing rate during different stimulus conditions: during spontaneous activity (gray screen, left) and throughout the entire recording session (right).
Author response image 2
RGC-SC connectivity.

Cross-correlograms showing 4 connected RGC-SC pairs (top) with two RGCs connecting onto the same SC neuron. Raster plots of SC neuron spiking activity in response to firing of the presynaptically …

Author response image 3
Change of mean paired-spike ratio (PSR) depending on ISI.

(Left) Comparison of PSR between two groups of different ISIs. The 2-30 ms group ensures to include high-firing RGCs (excitatory pairs 2-30 vs 5-30 ms p = 0.011; inhibitory pairs 2-30 vs 5-30 ms p = …

Author response image 4
Relationship between efficacy to 1st RGC and PSR visualized on linear scale using a hyperbolic fitting approach a/sinh(bx)+c.
Author response image 5
Relationship between RF size and connectivity measures (efficacy and contribution) for RGC-SC EXN and RGC-SC IN pairs (two-sided Wilcoxon rank-sum test).
Author response image 6
Mean firing rate (left) and RF size (right) as a function of peak-to-trough (PT) duration for excitatory and inhibitory SC neurons.

Both measures are not correlated to the PT duration (Pearson correlation coefficient, two-sided Wilcoxon rank-sum test).

Author response image 7
Functional estimation of probe location.

DiI staining of Neuropixels probe (middle) and multi-unit activity across channels in response to visual stimulation (bottom). The white dashed lines in the middle and bottom panels mark the rough …

Author response image 8
Optotagging approach.

Example traces of a single stimulation pulse and protocol used for optogenetic stimulation. Evoked activity in response to LED stimulation (100ms, 100 trials) for six example SC IN neurons.

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