The Potential Overlapping Roles of the Ear and Lateral Line in Driving “Acoustic” Responses

Abstract

Examination of fish responses to sound stimuli has a rich and varied history but it is not always clear when responses are true measures of hearing or the lateral-line. The central innervation of auditory and lateral-line sensory afferents lie in close proximity in the brainstem and both sets of receptors are, at heart, hair cell-based particle motion detectors. While it is possible to separately measure physiological activity of these two receptor subtypes, many studies of fish "hearing" use whole brain potentials or behavioural assays in complex sound fields where it is not possible to distinguish inputs. We argue here that, as often measured, what is thought of as fish "hearing" is often a multisensory response of both auditory and lateral line receptors. We also argue that in many situations where fish use sound stimuli, the behaviour is also an integrative response of both systems, due to the often close proximity of fish during sound communication. We end with a set of recommendations for better understanding the separate and combined roles of ear and lateral-line hair cells as well as an acknowledgment of the seminal and continuing contributions of Arthur N. Popper and Richard R. Fay to this field.

Mechanosensory Lateral Line Nerve Projections to Auditory Neurons in the Dorsal Descending Octaval Nucleus in the Goldfish, Carassius auratus

“…They suggest that published auditory evoked potentials in other species may well reflect the overlapping sensitivities of these two modalities at low frequencies [Higgs and Radford, 2016]. Indeed, responses to the lowfrequency components of species-specific vocalization have been demonstrated for the superficial LL neuromasts in the plainfin midshipman [Weeg and Bass, 2002] and for the ALLn in the related oyster toadfish [Radford and Mensinger, 2014].…”

“…Interaction between the two modalities may influence close-range mating or aggressive behaviors [Weeg and Bass, 2002;Higgs and Radford, 2016]. Braun and Coombs [2010] provided evidence in the mottled sculpin Cottus bairdi that the LL and auditory systems might be used either in series or in parallel according to specific behavioral contexts.…”

“…The local incompressible flows are capable of stimulating the mechanosensory LL at low frequencies ( ∼ 1-200 Hz) within short distances (within 1-2 body lengths of the fish). Therefore, if a fish is close to the source of sound/water movement with an upper limit of 200 Hz, both the mechanosensory LL and the otolithic end organs may be stimulated [reviewed in Coombs and Montgomery, 1999;Braun and Sand, 2014;Higgs and Radford, 2016].…”

Ecology of fish hearing

“…Sound travels more efficiently and greater distances underwater compared with air because the speed of sound in water is approximately five times faster, resulting in limited environmental attenuation due to absorption (Figure ; Higgs & Radford, ; Urick, ). Within approximately two wavelengths of the sound source, there is not a simple relationship between sound level and distance (nearfield) because sound pressure is not in phase with the particle motion component (Higgs & Radford, ). Whereas, within the far field, outside the nearfield region, particle motion is in phase with sound pressure and the sound level decreases by 6 dB for each doubling of distance from the source (Figure ).…”

“…Fluctuations near the source are due to source structure and would depend on direction. , Sound level for an ideal point source (adapted from Higgs & Radford, )…”