High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons

Abstract

The superior colliculus is a midbrain structure that plays important roles in visually guided behaviors in mammals. Neurons in the superior colliculus receive inputs from retinal ganglion cells but how these inputs are integrated in vivo is unknown. Here, we discovered that high-density electrodes simultaneously capture the activity of retinal axons and their postsynaptic target neurons in the superior colliculus, in vivo. We show that retinal ganglion cell axons in the mouse provide a single cell precise representation of the retina as input to superior colliculus. This isomorphic mapping builds the scaffold for precise retinotopic wiring and functionally specific connection strength. Our methods are broadly applicable, which we demonstrate by recording retinal inputs in the optic tectum in zebra finches. We find common wiring rules in mice and zebra finches that provide a precise representation of the visual world encoded in retinal ganglion cells connections to neurons in retinorecipient areas.

Efficient mapping of the thalamocortical monosynaptic connectivityin vivoby tangential insertions of high-density electrodes in cortex

“…The visual stimuli were displayed on a monitor screen (Dell, calibrated at refresh rate = 120 Hz, mean luminance = 120 cd/m 2 ). The stimulus set was made of: two sparse noise stimuli with either dark or light targets (15 deg size, 2 targets/frames of 100 ms, 20 repeats for each position on a grid of 36×22 squares), moving bars (white bars on black background, 10 deg in width, 12 directions, fixed speed of 90 deg/s), followed by the final full-field chirp stimulus 13 . For each exposed image, a logic electric signal was produced and sent to the digital-to-analog converter (NI-DAQmx connected in the NI-PXI with a PXI-8381) to support later re-alignment and re-interpolation of the time between the visual stimuli and the registered spike times.…”

“…In the pharmacological experiments ( n = 5 mice), an extra stability control is strongly advised to reject bad clusters including waveforms of different shapes in the different pharmacological conditions. This step was performed in a custom written GUI illustrating the MCW recalculated in each pharmacological condition separately 13 . Once all controls are finished, the amplitude and the spread of each cluster can be estimated .…”

“…Recording the activity of thalamic neurons at the axonal level within cortex, simultaneously with the activity of nearby cortical neurons, would overcome the challenging step of aligning multiple probes across distant brain regions and allow to map the thalamocortical connectivity in a more efficient manner. Recently, we showed that high-density electrodes (Neuropixels probes 12 ) capture the activity of retinal ganglion cell axons within the mouse superior colliculus, allowing a detailed characterization of the retinocollicular synaptic connectivity in vivo 13 . Here we investigated whether high-density electrodes can also record the activity of thalamic axons within cortex and thus allow to efficiently monitor and functionally map thalamocortical monosynaptic connections.…”

“…2g). Finally, we can estimate the spike transmission efficacy 13 providing an in vivo measure of the thalamocortical connection strength (Fig. 2h, median efficacy = 1.8 %, first quartile = 1.2 %, third quartile = 3.1 %, n = 208 connected pairs, n = 8 mice).…”

Birds multiplex spectral and temporal visual information via retinal On- and Off-channels

“…This is in part due to the difficulty of recording from the ex-vivo bird retina [19][20][21] , where minor mechanical insult causes pathological waves of depression 22 . Consequently, to date insights into the operation of avian retinas are largely 19,23 restricted to non-invasive techniques such as electroretinograms 24,25 .…”