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.
Xenopus laevis employs mechano-sensory lateral lines to, for instance, capture arthropods on the surface of turbid waters with poor visibility based on incoming wave signals. To characterise central representations of surface waves emitted from different locations, responses to several wave parameters were extracellularly recorded across brainstem, midbrain and thalamic areas. Overall, 339 of 411 statistically analysed responses showed significantly altered spike rates during the presentation of surface waves. Of these units, 45.1% were obtained in the torus semicircularis including its laminar subnucleus (23.3%) that is known to process auditory cues. Wave parameters contributing to central object representations were indicated by response rates that systematically varied with amplitude (76.3% of 160 tested units), frequency (74.4% of 270 tested units), source angle (93.7% of 79 tested units), or source distance (63.8% of 218 tested units). Map-like parameter representations were rather diffuse, yet an increased fraction of units tuned to frontal source angles was observed at deeper tissue layers (>180 μm), and an increased fraction of best neuronal responses to low wave frequencies (≤25 Hz) at rostral midbrain sections. Responses to wave frequencies remained largely robust across tested unit samples independent of source angles, and distances (N = 62). In comparison, spatial response characteristics seemed fragile across different wave frequencies in 68.3% of 41 recordings.
Aquatic predators like Xenopus laevis exploit mechano-sensory lateral lines to localise prey on the water surface by its wave emissions. In terms of distance, hypothetically, the source of a concentric wave could be centrally represented based on wave curvatures: for Xenopus, we present a first sample of 98 extracellularly recorded brainstem and midbrain responses to waves with curvatures ranging from 22.2-11.1 m(-1). At the frog, concurrently, wave amplitudes and their spectral composition were kept stable. Notably, 61% of 98 units displayed curvature-dependent spike rates, suggesting that wave curvatures could support an extraction of source distances in the amphibian brain.
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