The Synaptic Basis of Binocular Alignment and its Development in Ferret Primary Visual Cortex

Abstract

The brain integrates information from a myriad of external stimuli to generate a rich but consistent representation of the world and instruct behavior. For coherent binocular vision, signals from both eyes need to be combined to generate a unified percept. In visually experienced animals, neurons in primary visual cortex (V1) display highly similar responses to right and left eye stimulation, referred to as binocular alignment [1, 2, 3, 4, 5, 6, 7]. Yet, in visually naive animals, neurons exhibit more diverse responses for each eye and visual experience is required for improving binocular alignment and thereby refining binocular vision [4, 5, 8]. While studies have addressed the alignment process of neurons or networks, we still lack an understanding about the synaptic basis of binocular alignment. Two hypotheses ascribe contrasting importance to 1) feedforward driven convergence of monocular signals from each eye and 2) a binocular (driven by stimuli through either eye), recurrent, intracortical network in the alignment process. <br /> We used in-vivo two-photon functional imaging of dendritic spines of layer 2/3 (L2/3) neurons in ferret V1 to disentangle the contribution of monocular and binocular inputs. We probed the functional properties of dendritic spines and somata during right and left eye stimulation in ferrets with and without prior visual experience to uncover how somatic binocular responses are supported by excitatory synaptic inputs over development. <br /> We find that individual neurons receive a mixture of monocular and binocular synaptic inputs at both developmental stages. Amongst this diversity of inputs, we find a unique role for binocular congruent inputs. These spines exhibit strong tuning correlation between right and left eye responses and therefore convey input that is aligned between both eyes. Consistently across development, the more binocular congruent inputs a neuron receives, the more congruent its somatic output. Higher levels of somatic congruency after visual experience are attributed to a greater proportion of binocular congruent inputs relative to naive animals. The critical relevance of numbers of synapses is further highlighted by the fact that binocular congruent spines in experienced animals do not exhibit greater synaptic strength than noncongruent and monocular inputs. Lastly, it seems that the increase in numbers of binocular congruent inputs after eye opening transforms the dominant source of ipsilateral eye inputs. <br /> We conclude that binocular alignment in L2/3 of ferret V1 arises from biases in the synaptic interactions within a binocular, intracortical (recurrent) network, rather than the classic feedforward model in which monocular inputs become aligned. Over development, a numerically growing binocular congruent network overrides other sources of inputs from the ipsilateral eye inducing changes in somatic responses to the ipsilateral eye that are better aligned with the contralateral eye.