The emergence of selectivity in the mammalian neocortex by Nicolas Priebe

The question of how precise response selectivity emerges in the visual cortex has been marked by considerable controversy, ever since Hubel and Wiesel first described orientation selectivity. Today, there are essentially two opposing views of how selectivity arises. Feed-forward models, derived from Hubel and Wiesel’s original proposals, rely entirely on the properties and organization of thalamic, or feed-forward, inputs to cortical cells. Feed-back models require some form of lateral inhibition to refine response selectivity relative to the rather weak bias provided by thalamic inputs.

This debate has in large part been driven by the paradox presented by two divergent lines of evidence. On the one hand, many cortical response properties, such as cross-orientation suppression, orientation, direction and temporal frequency selectivities, appear to require lateral inhibition. On the other hand, while lateral inhibition could potentially provide considerable computational power to neuronal circuits, several lines of evidence suggest that it may not sharpen selectivity in the cerebral cortex. In intracellular recordings from primary sensory cortical areas in vivo, synaptic activity often lacks the necessary properties to support lateral inhibition. Specifically, inhibitory inputs are most often tuned to the same stimuli as the excitatory inputs, and inhibition evoked by non-preferred stimuli is generally weak. Additionally, inactivation of the cortical circuit, including both excitatory and inhibitory components, does not degrade the selectivity of the remaining feed-forward synaptic inputs.

I will present intracellular in vivo recordings that suggest a model for cortical computation that does not rely on lateral inhibition.  Instead, we can explain complex aspects of cortical responses parsimoniously from simple, well-characterized, nonlinear features of the feed-forward excitatory pathways, such as spike threshold, contrast saturation, and spike rectification, along with stimulus induced changes in background membrane potential fluctuations. These changes in the amplitude and frequency of membrane potential fluctuations alter the relationship between the average membrane potential and firing rate, and act as a gain control element that shapes cortical selectivity.

Nicolas Priebe is Professor at Department of Neuroscience University of Texas, Austin USA and is invited professor in the team of Cendra Agulhon in june 2019.