Abstract
Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species.
Highlights
How sensory neurons process incoming sensory input thereby leading to perception and behavior remains a central question in systems neuroscience
Data obtained from ON- and OFF-type electrosensory lateral line lobe (ELL) pyramidal neurons were pooled because, consistent with previous studies (Huang and Chacron, 2016), we found no overall difference between their responses to envelopes
We investigated the roles of both direct and indirect sources of descending input onto ELL pyramidal cells in determining their responses to envelopes
Summary
How sensory neurons process incoming sensory input thereby leading to perception and behavior remains a central question in systems neuroscience. Theory posits that efficient coding is achieved by ensuring that the neural tuning function is inversely proportional to stimulus intensity as a function of frequency, thereby achieving a neural response whose amplitude is independent of frequency (Rieke et al, 1996) While such ‘whitening’ has been observed across species and systems (Dan et al, 1996; Wang et al, 2003; Huang et al, 2016; Pozzorini et al, 2013; Pitkow and Meister, 2012), the nature of the underlying mechanisms remains unclear. Electric fish offer an attractive model system for studying the mechanisms underlying optimized coding of natural stimuli because of well-characterized anatomy and physiology (Clarke et al, 2015; Berman and Maler, 1999; Chacron et al, 2011). Electric fish give robust behavioral responses to movement related envelopes in which the EOD frequency tracks the stimulus’ detailed (Metzen and Chacron, 2014)
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