Hierarchical Sensory Guidance of Mauthner-Mediated Escape Responses in Goldfish (<i>Carassius auratus</i>) and Cichlids (<i>Haplochromis burtoni</i>)

Abstract

Acoustically-evoked escape behaviors were compared between goldfish (Carassius auratus), a hearing specialist, and the cichlid Haplochromis burtoni, a hearing nonspecialist. Fish were startled with compressive and rarefying, stimuli presented alone or together, and with compressive pulses preceded by a visual cue or after exposure to cobalt, an inhibitor of lateral line-innervated neuromast hair cells. These acoustic startle stimuli can evoke Mauthner neuron firing and are similar to but weaker than those produced by a largemouth bass (Micropterus salmoides) feeding on guppies. When sound stimuli were presented alone, both species avoided the direction of either the compressive or rarefying stimulus. If a light preceded and was contralateral to the compressive sound pulse, goldish continued to avoid the sound source; cichlids avoided the visual cue and turned toward the sound. Goldfish performance improved significantly when the visual cue was in the same direction as the sound source. Goldfish performance also improved significantly after exposure to 0.1 mmol I^-1 cobalt solution for 24 hours before testing, but cichlids would not startle after cobalt acclimation. A compressive pulse presented to one side of a fish simultaneously with a rarefying pulse on the other side causes the entire fish to accelerate with the water current. This strongly and directly accelerates the ear but tends to reduce both the pressure changes transduced by the swimbladder and activation of the mechanosensory lateral line. In this test, goldfish reliably avoided the compressive pulse. Cichlids, however, randomly avoided either speaker polarity but significantly avoided the speaker which had a faster onset. With more closely matched speakers, cichlids also preferentially avoided the compressive stimulus. Thus, the primitive sensory condition for auditory activation and guidance of Mauthner-neuron-initiated escape responses may have evolved to detect the initially compressive sounds associated with ram-type predators.

Development of the acoustically evoked behavioral response in zebrafish to pure tones

“…The adjustment in activation threshold is consistent with feedforward inhibition of the Mauthner-cell circuitry underlying escape responses in goldfish (for review see Faber et al, 1989) that can be potentiated by sound stimuli (Oda et al, 1998). Canfield and Rose (1996) reported that largemouth bass (Micropterus salmoides) feeding on guppies produce ~170·dB (re 1·µPa, ~200·Hz), and in the same paper used ~150·dB (re 1·µPa, ~500·Hz) to elicit escape responses from goldfish. From our measurements, both adult and larval zebrafish would respond to the bass strike and the ~150·dB (re 1·µPa, ~500·Hz) used to elicit responses from goldfish.…”

Preparing for escape: anti-predator posture and fast-start performance in gobies

“…Hence, receiving a weak ipsilateral stimulation (WS) prior to the startling stimulus did not increase the chances of responding away from the stimulus. In other fish species (goldfish Carassius auratus and cichlids Haplochromis burtoni) a directional visual stimulus displayed 10-100 ms prior to an acoustic non-directional startling stimulus was shown to affect escape direction, presumably by driving one of the Mauthner cells closer to firing threshold (Canfield, 2003;Canfield and Rose, 1996). In our experiment, the interval between WS and SS was relatively long (30 s), which may allow the Mauthner cells enough time to return to their normal firing threshold.…”

The contribution of the lateral line to 'hearing' in fish

“…Ablation of the lateral line increases the response latency of the 'acoustic' escape response in goldfish and alters the directionality of this response when tested with an underwater sound source , presumably due to electrical synapses with the Mauthner cells forming the motor aspects of the escape response . Interestingly, when goldfish startle responses are triggered with an airborne sound source, ablation of lateral line inputs improves escape responses (Canfield and Rose, 1996), suggesting that the relationship between particle motion and pressure waves in the stimulus can affect the relative role of the ear and lateral line. It is likely that in nature fish use inputs from both auditory and lateral line systems either simultaneously or in series (Braun and Coombs, 2000;Webb et al, 2008) to ascertain the true nature of 'sound' stimuli and make appropriate behavioural decisions.…”