Untangling Bottom-Up Activation and Top-Down Modulation in Visual Cortex with Multielectrode Extracellular Neuronal Recordings

Abstract

Visual perception arises from the combination of bottom-up (feedforward) activation and top-down (feedback) modulation of neuronal activity. Distinguishing these processes is challenging. Using multielectrode extracellular neuronal recordings, the activity of large populations of neurons can be studied simultaneously. Comparing across distinct, simultaneously-recorded neurons allows for the individual influences of each bottom-up activation and top-down modulation on cortical activation to be untangled. Using this approach, we found that in area V4, a visual region of the brain thought to be important for shape processing, neurons enhance their responses to an array of stimuli only when the array implies an occluding object. Simultaneously recorded neurons that represented the un-occluded parts of the stimulus array did not increase firing. This specificity suggests that V4 differentiates feedforward information about the illusion on a fine scale. These V4 neurons might provide feedback information to primary visual cortex (V1) to support the perception of the inferred stimulus. In V1, using a separate, cognitively demanding task, we found that feedback can both enhance and suppress stimulus-evoked spiking activity. This finding is significant as most feedback projections are excitatory in nature, while many models of visual processing rely on inhibitory top-down modulation. We further probed V1 by sending conflicting, bottom-up activation into the neuronal circuitry. We also found that conflicting bottom-up activation, whose resolution likely involves cortico-cortical feedback, results in distinct phases of excitation and inhibition across the local microcircuit that are in line with the assumption of feedback-induced inhibition of visual cortical responses. Taken together, these findings provide important new insights into the intra- and inter-areal interplay of bottom-up sensory information with top-down guided modulation of local neuronal processing.