Orientation preference is a prominent feature of the mammalian visual cortex, but the mechanisms underlying its development remain elusive. Spontaneous cortical activity is thought to play an important role in the maturation of orientation selectivity, yet it is still unclear how spontaneous activity shapes this process.
Here we address this question by combining chronic imaging experiments and computational analyses. We used GCaMP6s to image visually evoked responses with moving grating stimuli and spontaneous activity in ferret primary visual cortex, from four days prior to the natural time of eye-opening (~P30 in ferrets) until about a week after eye-opening. Prior to P30, the eye lids were transiently opened when probing the cortex with grating stimuli. This setup allows us to assess the emergence and refinement of orientation selectivity and its relationship to spontaneous activity during early development.
We found that, already at the earliest time point measured (P26), visual stimuli robustly evoke responses that are modular (i.e., patchy), extend over the whole field of view, and are highly variable across trials. Typically, weak orientation tuning is evident at this stage, but its layout only coarsely resembles the mature organisation. Indeed we observe considerable reorganisation until a near mature layout is reached a few days after eye-opening.
To determine if early spontaneous activity could drive the refinement of orientation preference, we built a correlation-based model of early visual cortex, assuming that locations with positively correlated spontaneous activity become more similar in their tuning at later stages in development, whereas negatively correlated locations become more dissimilar. Using the measured spontaneous correlation structure and layout of orientation preference in the early cortex, our model predicts aspects of the subsequent reorganization of orientation preference towards its mature layout. The model predicts that spontaneous activity and the orientation preference map become increasingly similar in their layout during development and we confirm this prediction with our experimental data. Thus, this correlation-based approach captures the refinement of orientation preference as well as of its relationship to spontaneous activity.
We conclude that early cortical spontaneous activity plays a significant role in driving the refinement of the circuits underlying orientation preference in visual cortex.