Organization of inhibitory synaptic circuits in layer 4 of ferret visual cortex related to direction preference maps

Simple cells in layer 4 of the primary visual cortex are the first neurons in the visual pathway showing orientation and direction selective responses. The precise role of intracortical excitatory and inhibitory connections in generating these properties is still unclear. Intracortical inhibitory processes have been shown to be crucial to the generation of direction selective responses. In vivo, excitatory and inhibitory layer 4 cells differ in their receptive field properties: excitatory (regular spiking) neurons are orientation- and direction selective whereas inhibitory (fast spiking) neurons are orientation-, but poorly direction tuned. This difference in direction tuning could be due to differences in intracortical inhibitory synaptic input patterns. To address this question we have optically recorded orientation and direction maps from ferret primary visual cortex. Subsequently the imaged brain region was removed and tangential slices prepared. Whole cell patch clamp recordings from individual layer 4 neurons were done and synaptic inputs were scanned by local photolysis of caged glutamate. Postsynaptic cells were filled with biocytin and histological sections were aligned with the synaptic input maps and the optical images obtained in vivo to determine the spatial distribution of presynaptic inputs. The majority (68%) of excitatory inputs to both spiny (excitatory) and aspiny (inhibitory) stellate cells originated from cortical regions preferring the same orientation and direction as the postsynaptic cell. However, the inhibitory input patterns were significantly different for the two cell populations: excitatory layer 4 cells received two populations of inhibitory inputs, about 50% originated in iso-direction domains whereas the remaining inputs originated in cortical regions preferring the opposite direction of stimulus motion. This indicates that specific inhibitory connections originating in regions tuned to the opposite direction are important for direction tuning of cortical neurons and that differences in response properties in different populations of cortical neurons might be explained by their different intracortical connectivity patterns.