Neural responses to water surface waves in the midbrain of the aquatic predator Xenopus laevis laevis

Abstract

Many aquatic vertebrates use mechano-sensory lateral lines to decipher water movements. The peripheral and central organization of the lateral line system has much in common with the auditory system. Therefore, it was hypothesized that the information processing of both systems could be related. Analogous to acoustic objects, for instance, object representations along the central lateral line pathway must be generated from patterns of particle motion across peripheral receivers. Thus, the lateral line offers insight into key features of neural computation beyond a specific sensory system. Here, central processing of water surface waves was described in the African clawed frog which depends on wave signals for prey detection, recognition and localization. Neural responses to surface wave stimuli were recorded in the brainstem and midbrain of Xenopus. A total of 109 units displayed either excitatory or inhibitory responses to surface waves. The response pattern distribution differed significantly across the optic tectum and torus semicircularis magnocellularis (chi-square test, P < 0.05). Stimulus frequencies from 10 to 40 Hz were represented equally across lateral line nuclei but best frequencies were systematically distributed along the rostrocaudal axis of the midbrain (chi-square test, P < 0.05). Forty-one percent of 102 widely distributed units phase locked significantly to stimulus frequencies (Rayleigh test, P < 0.05; vector strength > 0.3) and 41% of 39 tested units featured non-monotone rate-level functions. These neurones were registered mainly in the dorsal tectum and magnocellular torus semicircularis (chi-square test, P < 0.05). Across all tested nuclei, 16 of 17 discreetly distributed units showed a directional response to spatial stimulation. The results suggest midbrain subdivisions with respect to processing of stimulus timing, frequency and amplitude.