Precise endogenous control of involvement of right and left visual structures in assessment by zebrafish

Abstract

Birds and fish use monocular viewing to bring to bear appropriate lateralised specialisations. In larval zebrafish, persistent left eye (LE) viewing of their own reflection is interrupted by a series of brief ‘events’, in which the right eye has equal use. These recur with precise 160 s periodicity, with the first beginning after 40 s, and allow right and left mechanisms to assess the reflection.

In a strain in which persistent LE bias ceased after about 2 min, events were still marked by a brief period of frontal viewing, immediately after the time of each event (‘after-effects’). Such viewing allows simultaneous access by both right and left visual systems, and may be associated therefore with interaction, perhaps involving linkage of initially independent traces. Events appeared to cease after the maximal after-effect following the third event. Older fish show changes in overt behaviour immediately after event times; again the third event ends this. Processes associated with events thus progressively change what is available to recall.

Domestic chicks show enhanced evocation of response (e.g. sex, defense) to fellows, with the LE but not the right, if exposed to light during embryonic development. In zebrafish (where light may act by an epiphyseal route) we found that after dark development, viewing bias peaked at the time of each event, with LE use at the first and right at the second. The main factor determining the outcome of right/left competition appears here to be recency of access to viewing.

Introduction

Non-mammalian vertebrates tend to bring lateralised specialisations into action by viewing monocularly. These specialisations are likely to be chiefly mediated by structures contralateral to the eye in use, but in the absence of definitive evidence, the terms left eye, and right eye systems are used here (LE, RE; LES, RES). Two lateralised specialisations are particularly relevant. Typically [1], the RES is concerned with the visual control of response: in the zebrafish, for example, targets tend to be selected by the RE, and the RE is used during approach to target [2]. Throughout the tetrapod vertebrates, LE input more readily initiates intense response to fellows (e.g. attack, sex). Fish show an apparently corresponding response when viewing their reflection. A number of species of adult teleost fish persistently view their own reflection, seen for the first time, with the LE [3]; so also do larval zebrafish [4].

In domestic chick and zebrafish, these two behavioural asymmetries are linked during development, in that both are affected by the same factors. Any reversal of allocation affects both. In the zebrafish [5], they reverse sides when the parapineal shifts early in development from its normal position on the left of the epiphysis to the right. In the chick [6], both reverse when the normal exposure of the RE to light entering through the shell during incubation is experimentally changed to exposure of the LE. It thus seems that they both depend on the same brain asymmetry in both a fish and a bird. This is confirmed by the fact that in the absence of light during development both asymmetries disappear in the chick [7]. We show here that dark development has a similar effect in the zebrafish: marked RE as well as LE bias occurred during viewing the reflection as a result, whilst duration of interest was not affected. This finding allowed us to distinguish between different factors that affect eye use during viewing a reflection.

The predominant use of the eye system that is more interested in a stimulus presumably has the advantage that appropriate specialisations are brought to bear. In the mirror test, LES interest in species-specific properties is clearly important. Assessment and recording of properties are also important, as shown by progressive changes in viewing across the course of testing, and by the effect of changes in the properties of the reflection. Predominant use of one eye system has potential disadvantages for full assessment and recording of properties. This may explain the existence of an elaborate mechanism for the regulation of access by LES and RES in turn, which is the central finding of this study. A series of brief periods (‘events’), recurring with precise 160 s periodicity, and consistent across individuals and strains, were revealed by the interruption of LE bias by increased RE use. In a strain in which LE bias persisted throughout the 10-min test, five such events were revealed. They are named here by the 20 s bin in which they ended, and bins are also named by their last second.

In a second strain (Tup Long Fin: TupLF), persistent LE bias typically lasts for about 2 min. The first event was revealed as usual. Later ones were still clearly present but were marked by a brief after-effect, in which lateral viewing (such as is used in periods of LE bias) was replaced by frontal viewing. This allows both eyes to view simultaneously, and may therefore permit interaction between eye systems, leading (for example) to linkage of left and right memory traces.

Larval zebrafish (fry) of the TupLF strain that had developed in the dark (Da Isolates) showed a new pattern. Events were now marked by peaks of bias. Between them bias was reduced or absent, showing that the normal special interest of LES in the reflection was reduced or absent. Direction of bias alternated between events, suggesting that lack of recent access to viewing gave advantage in competition between eye systems during events. Events thus may be concerned with the elaboration of adequate memory traces.

Independence of processing between LES and RES is clear in birds, where the two eyes can simultaneously search for different targets [8]. In fish and chameleons RE and LE may alternately scan, suggesting alternation of control [9]. Even in macaques [10] and humans [11] ‘perceptual rivalry’ occurs, in which assessments alternate that are appropriate to the specialisations of right and left side mechanisms. Problems of elaboration and reconciliation of right and left traces may thus remain in mammals, and require timed regulation.