Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex

Non technical summary Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether this selectivity arises purely from mechanisms within the cortex itself, from the special way afferents from the thalamus project to the cortex or from the sharpening of a bias for orientation that already exists in the retina and the thalamus. Our experiments support the last of these three hypotheses. We used a special protocol to study both inhibitory and excitatory interactions within the cortex as well as in the thalamus and we find that the orientation selectivity may depend upon multiple mechanisms - including the thalamic biases for orientation and intracortical inhibition and excitation.Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether the selectivity arises from intracortical mechanisms, from the pattern of afferent connectivity from lateral geniculate nucleus (LGN) to cortical cells or from the sharpening of a bias that is already present in the responses of many geniculate cells. To investigate this, we employed a variation of an electrical stimulation protocol in the LGN that has been claimed to suppress intracortical inputs and isolate the raw geniculocortical input to a striate cortical cell. Such stimulation led to a sharpening of the orientation sensitivity of geniculate cells themselves and some broadening of cortical orientation selectivity. These findings are consistent with the idea that non-specific inhibition of the signals from LGN cells which exhibit an orientation bias can generate the sharp orientation selectivity of primary visual cortical cells. This obviates the need for an excitatory convergence from geniculate cells whose receptive fields are arranged along a row in visual space as in the classical model and provides a framework for orientation sensitivity originating in the retina and getting sharpened through inhibition at higher levels of the visual pathway.