Parallel pathways carrying direction-and orientation-selective retinal signals to layer 4 of the mouse visual cortex.

Parallel visual pathways from the retina to the primary visual cortex (V1) via the lateral geniculate nucleus are common to many mammalian species, including mice, carnivores, and primates. However, it remains unclear which visual features present in both retina and V1 may be inherited from parallel pathways versus extracted by V1 circuits in the mouse. Here, using calcium imaging and rabies circuit tracing, we explore the relationships between tuning of layer 4 (L4) V1 neurons and their retinal ganglion cell (RGC) inputs. We find that subpopulations of L4 V1 neurons differ in their tuning for direction, orientation, spatial frequency, temporal frequency, and speed. Furthermore, we find that direction-tuned L4 V1 neurons receive input from direction-selective RGCs, whereas orientation-tuned L4 V1 neurons receive input from orientation-selective RGCs. These results suggest that direction and orientation tuning of V1 neurons may be partly inherited from parallel pathways originating in the retina.

Parallel pathways carrying direction and orientation selective retinal signals to layer 4 of mouse visual cortex.

Parallel functional and anatomical visual pathways from the retina to primary visual cortex (V1) via the lateral geniculate nucleus (LGN) are common to many mammalian species, including mice, carnivores and primates. However, the much larger number of retinal ganglion cell (RGC) types that project to the LGN, as well as the more limited lamination of both the LGN and the thalamocortical-recipient layer 4 (L4) in mice, leaves considerable uncertainty about which visual features present in both retina and V1 might be inherited from parallel pathways versus extracted by V1 circuits in the mouse visual system. Here, we explored the relationships between functional properties of L4 V1 neurons and their RGC inputs by taking advantage of two Cre-expressing mouse lines - Nr5a1-Cre and Scnn1a-Tg3-Cre - that each label functionally and anatomically distinct populations of L4 neurons. Visual tuning properties of L4 V1 neurons were evaluated using Cre-dependent expression of GCaMP6s followed by 2-photon calcium imaging. RGCs providing input to these neurons (via LGN) were labeled and characterized using Cre-dependent trans-synaptic retrograde labeling with G-deleted rabies virus. We find significant differences in the tuning of Nr5a1-Cre versus Scnn1a-Tg3-Cre neurons for direction, orientation, spatial frequency, temporal frequency, and speed. Strikingly, a subset of the RGCs had tuning properties that matched the direction and orientation tuning properties of the L4 V1 neurons to which they provided input. Altogether, these results suggest that direction and orientation tuning of V1 neurons may be at least partly inherited from parallel pathways originating in the retina.

Diversity in spatial frequency, temporal frequency, and speed tuning across mouse visual cortical areas and layers.

The mouse visual system consists of several visual cortical areas thought to be specialized for different visual features and/or tasks. Previous studies have revealed differences between primary visual cortex (V1) and other higher visual areas, namely, anterolateral (AL) and posteromedial (PM), and their tuning preferences for spatial and temporal frequency. However, these differences have primarily been characterized using methods that are biased toward superficial layers of cortex, such as two-photon calcium imaging. Fewer studies have investigated cell types in deeper layers of these areas and their tuning preferences. Because superficial versus deep-layer neurons and different types of deep-layer neurons are known to have different feedforward and feedback inputs and outputs, comparing the tuning preferences of these groups is important for understanding cortical visual information processing. In this study, we used extracellular electrophysiology and two-photon calcium imaging targeted toward two different layer 5 cell classes to characterize their tuning properties in V1, AL, and PM. We find that deep-layer neurons, similar to superficial layer neurons, are also specialized for different spatial and temporal frequencies, with the strongest differences between AL and V1, and AL and PM, but not V1 and PM. However, we note that the deep-layer neuron populations preferred a larger range of SFs and TFs compared to previous studies. We also find that extratelencephalically projecting layer 5 neurons are more direction selective than intratelencephalically projecting layer 5 neurons.