Going with, then against the flow: evidence against the optomotor hypothesis of fish rheotaxis

Abstract

Movement through an environment provides sighted organisms with dynamic visual cues known as optic flow. In flying insects, optic flow is important for collision avoidance, flight speed control and landing manoeuvres. The function of optic flow is much less understood in other taxa, particularly in fish. Despite a lack of quantitative studies, optomotor responses (OMRs) to optic flow are presumed to be nearly ubiquitously important for rheotaxis (orientation to currents), a widespread behaviour that confers a number of benefits, including energy conservation. Here we show that while very young larval zebrafish, Danio rerio, exhibit positive OMRs (swim in the direction of optic flow), thereby minimizing optic flow on the retina, older larvae and adults exhibit negative OMRs that increase optic flow. While the reason for this reversal remains unclear, negative OMRs are inconsistent with optically driven positive rheotaxis (orienting upstream). Furthermore, when optic flow cues are placed in conflict with nonvisual (mechanical) cues generated by water currents, adult fish largely ignore the optic flow cues relying instead on nonvisual cues. These results challenge a century-old belief that optic flow and the resulting OMRs are a dominant sensorimotor mechanism in rheotaxis, highlighting the importance of future work on life history changes in OMRs and the possible modulatory influence of learned, multisensory expectations.

Microfluidic Transportation Control of Larval Zebrafish through Optomotor Regulations under a Pressure-Driven Flow

“…Moreover, the paired t-test further depicted that there was a statistically significant difference in the transportation time with the presence and absence of visual cues (paired sample t-test, p-value < 0.01), indicating the dominance of visual cues over hydromechanical cues even within the microfluidic environment. This agrees well with the literature, where authors have highlighted that within open channels, visual cues dominate larval behavior [14,16,17]. However, it was further observed that with the sole presence of hydromechanical cues, zebrafish larvae could be transported efficiently within the microfluidic environment at relatively higher flow rates of 0.2 and 0.3 mL/min.…”

“…Although it is far from fully understanding the complicated behavioral dynamics of zebrafish larvae, the research fraternity widely believes that the lateral line of the zebrafish body mediates the orientation of the body against incoming flow and that the optomotor response (OMR) mediates counterflow [14][15][16][17]. In their natural surroundings, velocity gradients are created through nearby obstructions when the zebrafish larvae encounter a sheared flow.…”

“…In a recent review, the authors specified that optic flow behavior can be integrated with hydromechanical behavior to describe the multisensory behaviors of zebrafish larvae [16]. Very few studies have been conducted from this aspect with conventional experimental assays, suggesting that optic flow modalities dominate the behavioral responses of zebrafish larvae when they are available [14,17]. Still, the collaborative results from previous studies in terms of both cues in a microfluidic environment remain unclear; however, they will be beneficial for animal testing if they can be addressed in a systematic manner.…”

Zebrafish Aging Models and Possible Interventions

“…These findings support the view that zebrafish visual system and perception (in particular, motion perception) rely on similar principles commonly found in humans. On the other hand, although there are studies comparing larval responses to visual stimulation (e.g., motion) with that of adult zebrafish [49], there is almost no systematic investigation on perceptual changes during aging. Future studies examining age-related changes in zebrafish perception and perceptual acuity will be informative in this respect and are currently being performed in our laboratory.…”

Sparse coding predicts optic flow specificities of zebrafish pretectal neurons

“…Optic flow. Like many other animals, zebrafish larvae generate optokinetic responses of the eyes (OKR) and optomotor responses of the body (OMR) when exposed to visual stimuli simulating egomotion of the fish [2,8]. Both eye-and body movements generate space-variant patterns of local motion vectors on the retina which then have to be analyzed by subsequent processing stages.…”