Neuronal activity is not required for the initial formation and maturation of visual selectivity

Abstract

Neuronal activity is important for the functional refinement of neuronal circuits in the early visual system. At the level of the cerebral cortex, however, it is still unknown whether the formation of fundamental functions such as orientation selectivity depends on neuronal activity, as it has been difficult to suppress activity throughout development. Using genetic silencing of cortical activity starting before the formation of orientation selectivity, we found that the orientation selectivity of neurons in the mouse visual cortex formed and matured normally despite a strong suppression of both spontaneous and visually evoked activity throughout development. After the orientation selectivity formed, the distribution of the preferred orientations of neurons was reorganized. We found that this process required spontaneous activity, but not visually evoked activity. Thus, the initial formation and maturation of orientation selectivity is largely independent of neuronal activity, and the initial selectivity is subsequently modified depending on neuronal activity.

The Wiring of Developing Sensory Circuits—From Patterned Spontaneous Activity to Synaptic Plasticity Mechanisms

“…Importantly, visual experience is required for this maturation (Li et al, 2006). Seemingly in contrast, in the mouse, Hagihara et al (2015) found that the proportion of responsive and orientation-selective cells is mature at eye opening. This is in line with findings from Ko et al (2013) but unlike Rochefort et al (2011) where a gradual increase in responsiveness and selectivity was reported.…”

“…This early selectivity is independent of any visual experience as it is not prevented by dark-rearing (Rochefort et al, 2011), suggesting that spontaneous activity may mediate orientation and direction selectivity. Surprisingly, a recent study found that blocking spontaneous activity during development in mice did not reduce orientation selectivity (Hagihara et al, 2015). Spontaneous activity was blocked in L2/3 of the visual cortex, by expressing the inward rectifying potassium channel Kir 2.1 through in utero electroporation.…”

“…This is in line with findings from Ko et al (2013) but unlike Rochefort et al (2011) where a gradual increase in responsiveness and selectivity was reported. At eye opening, there is a bias for cells to respond to lines with a 90° angle (Rochefort et al, 2011; Hagihara et al, 2015). This bias is equalized after eye opening, which depends on activity but, critically, does not require visual experience (Hagihara et al, 2015).…”

“…At eye opening, there is a bias for cells to respond to lines with a 90° angle (Rochefort et al, 2011; Hagihara et al, 2015). This bias is equalized after eye opening, which depends on activity but, critically, does not require visual experience (Hagihara et al, 2015). It seems that the development of direction and orientation tuning is challenging to directly compare between the ferret and mouse.…”

“…Given that clonally related cells show similar orientation preferences (Li et al, 2012; Ohtsuki et al, 2012), these findings may have significant consequences for our understanding of visual development. It is important to consider that blocking spontaneous activity during the age at which the system transitions from gap-junction to chemical synapse signaling did not prevent normal orientation tuning (Hagihara et al, 2015). Together, these studies emphasize the importance of future studies to outline where spontaneous activity is, and is not, necessary for sensory development.…”