Are single-peaked tuning curves tuned for speed rather than accuracy?

Abstract

According to the efficient coding hypothesis, sensory neurons are adapted to provide maximal information about the environment, given some biophysical constraints. In early visual areas, stimulus-induced modulations of neural activity (or tunings) are predominantly single-peaked. However, periodic tuning, as exhibited by grid cells, has been linked to a significant increase in decoding performance. Does this imply that the tuning curves in early visual areas are sub-optimal? We argue that the time scale at which neurons encode information is imperative to understanding the advantages of single-peaked and periodic tuning curves. Here, we show that the possibility of catastrophic (large) errors creates a trade-off between decoding time and decoding ability. We investigate how decoding time and stimulus dimensionality affect the optimal shape of tuning curves for removing catastrophic errors. In particular, we focus on the spatial periods of the tuning curves for a class of circular tuning curves. We show an overall trend for minimal decoding time to increase with increasing Fisher information, implying a trade-off between accuracy and speed. This trade-off is reinforced whenever the stimulus dimensionality is high, or there is ongoing activity. Thus, given constraints on processing speed, we present normative arguments for the existence of the single-peaked tuning organization observed in early visual areas.