Mechanism underpinning the sharpening of orientation and spatial frequency selectivities in the tree shrew (Tupaia belangeri) primary visual cortex.

Most neurons in the primary visual cortex (V1) of mammals show sharp orientation selectivity and band-pass spatial frequency tuning. Here, we examine whether sharpening of the broad tuning that exists subcortically, namely in the retina and the lateral geniculate nucleus (LGN), underlie the sharper tuning seen for both the above features in tree shrew V1. Since the transition from poor feature selectivity to sharp tuning occurs entirely within V1 in tree shrews, we examined the orientation selectivity and spatial frequency tuning of neurons within individual electrode penetrations. We found that most layer 4 and layer 2/3 neurons in the same cortical column preferred the same stimulus orientation. However, a subset of layer 3c neurons close to the layer 4 border preferred near orthogonal orientations, suggesting that layer 2/3 neurons may inherit the orientation preferences of their layer 4 input neurons and also receive cross-orientation inhibition from layer 3c neurons. We also found that layer 4 neurons showed sharper orientation selectivity at higher spatial frequencies, suggesting that attenuation of low spatial frequency responses by spatially broad inhibition acting on layer 4 inputs to layer 2/3 neurons can enhance both orientation and spatial frequency selectivities. However, in a proportion of layer 2/3 neurons, the sharper tuning of layer 2/3 neurons appeared to arise also or even mainly from inhibition specific to high spatial frequencies acting on the layer 4 inputs to layer 2/3. Overall, our results are consistent with the suggestion that in tree shrews, sharp feature selectivity in layer 2/3 can be established by intracortical mechanisms that sharpen biases observed in layer 4, which are in turn inherited presumably from thalamic afferents.

Diversity of Feature Selectivity in Macaque Visual Cortex Arising from a Limited Number of Broadly Tuned Input Channels.

Spike (action potential) responses of most primary visual cortical cells in the macaque are sharply tuned for the orientation of a line or an edge, and neurons preferring similar orientations are clustered together in cortical columns. The preferred stimulus orientation of these columns span the full range of orientations, as observed in recordings of spikes and in classical optical imaging of intrinsic signals. However, when we imaged the putative thalamic input to striate cortical cells that can be seen in imaging of intrinsic signals when they are analyzed on a larger spatial scale, we found that the orientation domain map of the primary visual cortex did not show the same diversity of orientations. This map was dominated by just the one orientation that is most commonly preferred by neurons in the retina and the lateral geniculate nucleus. This supports cortical feature selectivity and columnar architecture being built upon feed-forward signals transmitted from the thalamus in a very limited number of broadly tuned input channels.