Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray

The mechanotactile hypothesis proposes that ventral non-pored lateral line canals in the stingray function to facilitate localization of prey that contact the skin during benthic feeding. This study used comparative neurophysiological and morphological techniques to test whether ventral non-pored canals encode the velocity of skin movements, and show other adaptations that may enhance detection of tactile stimuli from their prey. Resting discharge rate of lateral line primary afferent neurons was lower among units from ventral than dorsal canal groups. The ventral non-pored canals had a higher proportion of silent units (31%) than either ventral (3%) or dorsal (13%) pored canals, thus may have an enhanced potential for detection of phasic contact with prey. Primary afferents from pored canals showed response characteristics consistent with acceleration detectors, with best frequencies of 20-30 Hz. In contrast, units from non-pored canals responded to tactile skin depression velocities of 30-630 microm s(-1) from 1-20 Hz, and encoded the velocity of canal fluid induced by skin movement with best frequencies of < or =10 Hz. Sensitivity of non-pored canals to direct skin depression velocity was 2-10 times greater than to hydrodynamic dipole stimulation near the skin. No morphological specialization of hair cell orientation was found among pored and non-pored canals. These low frequency, tactile response properties support the hypothesis that the stingray's non-pored ventral lateral line functions as a mechanotactile receptor subsystem used to guide small benthic invertebrates to the ventrally positioned mouth.