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.

Development of Multisensory Convergence in the Xenopus Optic Tectum

“…It would be intriguing to know whether similar mechanisms are at play in the hindbrain input. For example, in the mature tectum, different populations of cells can be found that respond to either single sensory modalities or to different combinations (Behrend et al 2006;Lowe 1987). In our study, we found that all cells that receive input from retinotectal synapses also receive hindbrain inputs.…”

“…Much like its mammalian homologue, the superior colliculus, the optic tectum also receives inputs from a variety of different sensory modalities, including a range of mechanosensory inputs carrying somatosensory, auditory, vestibular, and lateralline information (Behrend et al 2006;Lowe 1986Lowe , 1987Munoz et al 1995;Vanegas 1984). In the colliculus, convergence between different sensory inputs can lead to multisensory integration, a process important for enhancing detection, localization, identification, and response to external environmental events (for a review, see Stein et al 2009).…”

“…Inputs from the various mechanosensory modalities, in contrast, terminate within the deeper layers (Behrend et al 2006;Lowe 1986Lowe , 1987Munoz et al 1995). In adult Xenopus, auditory and lateral-line inputs reach the tectum both via the torus semicircularis, a structure analogous to the mammalian inferior colliculus (Will et al 1985a,b;Zittlau et al 1988), and from direct inputs from medullary nuclei in the hindbrain that receive VIIIth (dorsal medullary nucleus) and lateral-line (lateral line nucleus) nerve inputs (Lowe 1986;Will et al 1985a,b).…”

Hydrodynamic discrimination of wakes caused by objects of different size or shape in a harbour seal (Phoca vitulina)

“…Several studies have described the capability of various aquatic animals, such as fishes and amphibians, to locate the sources of surface waves and subsurface water movements (e.g. Bleckmann et al, 1989;Coombs and Fay, 1993;Behrend et al, 2006;Görner, 1973) and to discriminate between parameters such as stimulus frequency (Bleckmann et al, 1981;Frühbeis, 1984;Elepfandt et al, 1985), amplitude (Waldner, 1981;Coombs and Fay, 1993) and object size (Vogel and Bleckmann, 2001). Furthermore, it has been shown that blind cave fishes are able to identify and discriminate the shape and spatial arrangement of stationary objects by means of lateral-line input (e.g.…”

The horizontal brain slice preparation: a novel approach for visualizing and recording from all layers of the tadpole tectum

“…THE AMPHIBIAN OPTIC TECTUM, homologous to the mammalian superior colliculus, is a multisensory processing center that receives visual input from the retinal ganglion cells (RGCs) in the eye as well as from nonoptic mechanosensory inputs originating from the somatosensory, lateral line, auditory, and vestibular systems (Behrend et al 2006;Lowe 1986;Munoz et al 1995). The neurons that comprise the optic tectum, collectively referred to as tectal neurons, organize into somatic layers with the deepest layer being the most periventricular and most medial.…”