Adaptation to second order stimulus features by electrosensory neurons causes ambiguity

Understanding the coding strategies used to process sensory input remains a central problem in neuroscience. Growing evidence suggests that sensory systems process natural stimuli efficiently by ensuring a close match between neural tuning and stimulus statistics through adaptation. However, adaptation causes ambiguity as the same response can be elicited by different stimuli. The mechanisms by which the brain resolves ambiguity remain poorly understood. Here we investigated adaptation in electrosensory pyramidal neurons within different parallel maps in the weakly electric fish Apteronotus leptorhynchus. In response to step increases in stimulus variance, we found that pyramidal neurons within the lateral segment (LS) displayed strong scale invariant adaptation whereas those within the centromedial segment (CMS) instead displayed weaker degrees of scale invariant adaptation. Signal detection analysis revealed that strong adaptation in LS neurons significantly reduced stimulus discriminability. In contrast, weaker adaptation displayed by CMS neurons led to significantly lesser impairment of discriminability. Thus, while LS neurons display adaptation that is matched to natural scene statistics, thereby optimizing information transmission, CMS neurons instead display weaker adaptation and would instead provide information about the context in which these statistics occur. We propose that such a scheme is necessary for decoding by higher brain structures.