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In the vertebrate visual system, all output of the retina is carried by retinal ganglion cells. Each type encodes distinct visual features in parallel for transmission to the brain. How many such 'output channels' exist and what each encodes are areas of intense debate. In the mouse, anatomical estimates range from 15 to 20 channels, and only a handful are functionally understood. By combining two-photon calcium imaging to obtain dense retinal recordings and unsupervised clustering of the resulting sample of more than 11,000 cells, here we show that the mouse retina harbours substantially more than 30 functional output channels. These include all known and several new ganglion cell types, as verified by genetic and anatomical criteria. Therefore, information channels from the mouse eye to the mouse brain are considerably more diverse than shown thus far by anatomical studies, suggesting an encoding strategy resembling that used in state-of-the-art artificial vision systems.

In the mouse, the parallel output of more than 30 functional types of retinal ganglion cells (RGCs) serves as the basis for all further visual processing. Little is known about how the representation of visual information changes between the retina and the dorsolateral geniculate nucleus (dLGN) of the thalamus, the main relay station between the retina and cortex. Here, we functionally characterized responses of retrogradely labeled dLGN-projecting RGCs and dLGN neurons to the same set of visual stimuli. We found that many of the previously identified functional RGC types innervate the dLGN, which maintained a high degree of functional diversity. Using a linear model to assess functional connectivity between RGC types and dLGN neurons, we found that the responses of dLGN neurons could be predicted as a linear combination of inputs from on average five RGC types, but only two of those had the strongest functional impact. Thus, mouse dLGN receives input from a diverse population of RGCs with limited functional convergence.

Mouse vision is based on the parallel output of more than 30 functional types of retinal ganglion cells (RGCs). Little is known about how representations of visual information change between retina and dorsolateral geniculate nucleus (dLGN) of the thalamus, the main relay between retina and cortex. Here, we functionally characterized responses of retrogradely labeled dLGN-projecting RGCs and dLGN neurons to the same set of visual stimuli. We found that many of the previously identified functional RGC types innervate dLGN, which maintained a high degree of functional diversity. Using a linear model to assess functional connectivity between RGC types and dLGN neurons, we found that responses of dLGN neurons could be predicted as linear combination of inputs from on average five RGC types, but only two of those had the strongest functional impact. Thus, mouse dLGN receives functional input from a diverse population of RGC types with limited convergence.

A fundamental challenge in calcium imaging has been to infer spike rates of neurons from the measured noisy fluorescence traces. We systematically evaluate different spike inference algorithms on a large benchmark dataset (>100.000 spikes) recorded from varying neural tissue (V1 and retina) using different calcium indicators (OGB-1 and GCaMP6). In addition, we introduce a new algorithm based on supervised learning in flexible probabilistic models and find that it performs better than other published techniques. Importantly, it outperforms other algorithms even when applied to entirely new datasets for which no simultaneously recorded data is available. Future data acquired in new experimental conditions can be used to further improve the spike prediction accuracy and generalization performance of the model. Finally, we show that comparing algorithms on artificial data is not informative about performance on real data, suggesting that benchmarking different methods with real-world datasets may greatly facilitate future algorithmic developments in neuroscience.

SummaryPrimary visual cortex (V1) exhibits two types of gamma rhythm: broadband activity in the 30–90 Hz range, and a narrowband oscillation seen in mice at frequencies close to 60 Hz. We investigated the sources of the narrowband gamma oscillation, the factors modulating its strength, and its relationship to broadband gamma activity. Narrowband and broadband gamma power were uncorrelated. Increasing visual contrast had opposite effects on the two rhythms: it increased broadband activity, but suppressed the narrowband oscillation. The narrowband oscillation was strongest in layer 4, and was mediated primarily by excitatory currents entrained by the synchronous, rhythmic firing of neurons in the lateral geniculate nucleus (LGN). The power and peak frequency of the narrowband gamma oscillation increased with light intensity. Silencing the cortex optogenetically did not affect narrowband oscillation in either LGN firing or cortical excitatory currents, suggesting that this oscillation reflects unidirectional flow of signals from thalamus to cortex.Highlights•Local field potential in mouse primary visual cortex exhibits a pronounced narrowband gamma oscillation close to 60 Hz.•Narrowband gamma is highest in the thalamorecipient layer 4•Narrowband gamma increases with light intensity and arousal state, and is suppressed by visual contrast.•Lateral geniculate nucleus neurons fire synchronously at the narrowband gamma frequency, independent of V1 activity.

Summary Primary visual cortex exhibits two types of gamma rhythm: broadband activity in the 30–90 Hz range and a narrowband oscillation seen in mice at frequencies close to 60 Hz. We investigated the sources of the narrowband gamma oscillation, the factors modulating its strength, and its relationship to broadband gamma activity. Narrowband and broadband gamma power were uncorrelated. Increasing visual contrast had opposite effects on the two rhythms: it increased broadband activity, but suppressed the narrowband oscillation. The narrowband oscillation was strongest in layer 4 and was mediated primarily by excitatory currents entrained by the synchronous, rhythmic firing of neurons in the lateral geniculate nucleus (LGN). The power and peak frequency of the narrowband gamma oscillation increased with light intensity. Silencing the cortex optogenetically did not abolish the narrowband oscillation in either LGN firing or cortical excitatory currents, suggesting that this oscillation reflects unidirectional flow of signals from thalamus to cortex., Highlights • Mouse V1 exhibits a pronounced narrowband gamma oscillation close to 60 Hz • This oscillation is strongest in layer 4 and specific to excitatory currents • It increases with arousal and light intensity and decreases with visual contrast • It is seen in lateral geniculate neurons, regardless of V1 activity, Saleem et al. discover that the narrowband gamma oscillation close to 60 Hz prevalent in the mouse visual cortex is inherited from the visual thalamus. The oscillation is enhanced by arousal and light intensity, and suppressed by visual contrast.