Internal gain modulations, but not changes in stimulus contrast, preserve the neural code

Neurons in primary visual cortex (V1) are strongly modulated both by stimulus contrast and by fluctuations of internal inputs. An important question is whether population codes are preserved under these conditions. Changes in stimulus contrast are thought to leave population codes invariant, whereas the effect of internal gain modulations remains unknown. To address these questions we studied how the direction-of-motion of oriented gratings is encoded in layer 2/3 primary visual cortex of mouse (with C57BL/6 background, of either sex). Surprisingly, we found that, because contrast gain responses across cells are heterogeneous, a change in contrast alters the information distribution profile across cells leading to a violation of contrast invariance. Remarkably, internal input fluctuations that cause commensurate firing rate modulations at the single-cell level result in more homogeneous gain responses, respecting population code invariance. These observations have important implications for visual information encoding and argue that the brain strives to maintain the stability of the neural code in the face of fluctuating internal inputs. SIGNIFICANCE STATEMENT While it is known that neuronal responses are modulated by both external and internal inputs, it is little known how these two different inputs impact population codes. Here, we explored effects of neuronal gain modulation derived by the two distinct inputs in population codes with specifying changes in stimulus contrast and spontaneous fluctuation of neuronal response as each type of external and internal input modulation. We showed that changes in stimulus contrast lead to different optimal codes while spontaneous internal input fluctuations leave the code invariant. This difference resulted from that changes in stimulus contrast modulate neuronal responses more heterogeneously across cells than spontaneous internal input fluctuation.