Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes

Accurate sensory perception often depends on the independent encoding and subsequent integration of multiple stimulus attributes. In the weakly electric fish Eigenmannia, P- and T-type primary afferent fibers are specialized for encoding the amplitude and phase, respectively, of electrosensory stimuli. We used a stimulus estimation technique to quantify the ability of P- and T-units to encode random modulations in amplitude and phase. As expected, P-units exhibited a clear preference for encoding amplitude modulations, whereas T-units exhibited a clear preference for encoding phase modulations. Surprisingly, both types of afferents also encoded their nonpreferred stimulus attribute when it was presented in isolation or when the preferred stimulus attribute was sufficiently weak. Because afferent activity can be affected by modulations in either amplitude or phase, it is not possible to unambiguously distinguish between these two stimulus attributes by observing the activity of a single afferent fiber. Simple model neurons with a preference for encoding either amplitude or phase also encoded their nonpreferred stimulus attributewhenit was presented in isolation, suggesting that such ambiguity is unavoidable. Using the well known jamming avoidance response as a probe of electrosensory perception, we show that the ambiguity at the single-neuron level gives rise to a systematic misrepresentation of stimuli at the population level and a resulting misperception of the amplitude and phase of electrosensory stimuli.