The function of fin rays as proprioceptive sensors in fish

Abstract

The sensation of movement and position of the limbs is critical for normal behaviours in tetrapods. In the bony fishes it is unclear what proprioceptive feedback is provided from the paired fins, the piscine homologues of the tetrapod limbs. Here we test mechanosensory abilities of afferent nerves in the pectoral fin rays, limb structures used by many fish species in propulsion and manoeuvreing. We examine the bluegill sunfish, a fish that uses its pectoral fins extensively in locomotion. We find that the activity of fin ray nerve fibres reflects the amplitude and velocity of fin ray bending. Spike sorting analyses demonstrate the presence of both slowly and rapidly adapting afferent nerve fibres. The fin sensory abilities we describe substantially expand the diversity of known vertebrate proprioceptive capabilities, and suggest that the pectoral fins need to be considered as possible proprioceptive sensors in studies of their functional morphology, movement and evolution.

Pectoral fins aid in navigation of a complex environment by bluegill sunfish under sensory deprivation conditions

“…Recent neurobiological studies have found that bluegill sunfish have putative mechanosensitive nerve endings in the distal ends of their pectoral fins and that these structures convey feedback in response to bending of the pectoral fin rays (Hale and Williams, 2012;Williams et al, 2013). This is a particularly exciting finding in light of extensive research that has failed to find proprioceptive receptors in fish with non-specialized fins (like those in bluegill sunfish) capable of providing sensory information regarding hydrodynamic loading (Ballintijn, 1972;Bone, 1978;Ono, 1979).…”

Flowing water affects fish fast-starts: escape performance of the Hawaiian stream goby,Sicyopterus stimpsoni

“…In contrast, proprioceptive capacity of the fins (e.g. caudal fin) may facilitate responses to flow pulses from the caudal direction that oppose ambient flow (Flammang and Lauder, 2013;Williams et al, 2013). The strength of a stimulus relative to the strength of alternative environmental cues has been shown to influence the type and number of escape responses in animals, including fish (Abrahams and Kattenfeld, 1997;Domenici, 2010a; D. G. Roche, Effects of biotic and physical stressors on fish swimming performance and behavior, PhD thesis, Australian National University, 2014).…”

Fin ray sensation participates in the generation of normal fin movement in the hovering behavior of the bluegill sunfish (Lepomis macrochirus).

“…This study adds taxonomic breadth to the body of work on the role of sensation in movement of vertebrate limbs and shows that sensorimotor integration in limb movement is a more general feature of animals than previously known. Although deafferentation removes all modes of sensory feedback from the rays and membrane of the fins, given the known proprioceptive capacity of fin ray nerves in fish (Williams et al, 2013) and the importance of mechanosensation in limb movement of other taxa (e.g. Gray and Lissmann, 1940;Abelew, 2000;Stevenson and Kutsch, 1986, 1988, we believe that the changes we see primarily result from the loss of mechanosensory feedback.…”

“…In bluegill sunfish (Lepomis macrochirus Rafinesque 1819), afferent nerves in the fin rays and membrane can convey proprioceptive feedback that reflects fin ray position and velocity at frequencies and bend amplitudes consistent with fin movement in swimming and hovering (Williams et al, 2013). Although not exploring movement or stability, several studies suggest the general importance of fin ray mechanosensation in behavior.…”

“…Afferents spike phasically with the wing beat cycle at typical wing beat frequencies (Dickinson, 1990b). Both of these features, adaptation properties and activity within a movement cycle, also appear to characterize mechanosensation by fish fins (Williams et al, 2013).…”