Noam Miller

Quantification of shoaling behaviour in zebrafish (Danio rerio)

Zebrafish has been a favourite of developmental biologists and numerous genetic tools have been developed for this species. In recent years, zebrafish has become an increasingly popular subject of neuroscientists and behavioural scientists. One of the typical characteristics of zebrafish is shoaling, individuals forming a tight group in which fish swim together. The biological mechanisms of social behaviours are complex and not well understood in vertebrates, and zebrafish, due to its highly social nature and the genetic tools developed for it, may represent an excellent animal model with which these mechanisms may be studied. Improvement of behavioural quantification methods would facilitate research in this area. We describe a custom software application that allows the precise quantification of several parameters of group cohesion in zebrafish. We also present three experimental examples to illuminate the use of our methodology, and show how group cohesion changes in response to manipulations of the environment.

Learning about environmental geometry: an associative model.

K. Cheng (1986) suggested that learning the geometry of enclosing surfaces takes place in a geometric module blind to other spatial information. Failures to find blocking or overshadowing of geometry learning by features near a goal seem consistent with this view. The authors present an operant model in which learning spatial features competes with geometry learning, as in the Rescorla-Wagner model. Relative total associative strength of cues at a location determines choice of that location and thus the frequencies of reward paired with each cue. The model shows how competitive learning of local features and geometry can appear to result in potentiation, blocking, or independence, depending on enclosure shape and kind of features. The model reproduces numerous findings from dry arenas and water mazes.

Oscillations in shoal cohesion in zebrafish (Danio rerio)

In many species, group cohesion may be the result of a compromise between opposing forces (e.g. predator avoidance and competition for food). However, little empirical data exists on the dynamics of group cohesion. We present moment-to-moment positional data on zebrafish shoals and analyze temporal changes in inter-individual distances. We demonstrate that the distance between shoal members does not settle at any given value, as has previously been assumed, but oscillates with a period between 5 and 15s.

Both information and social cohesion determine collective decisions in animal groups

During consensus decision making, individuals in groups balance personal information (based on their own past experiences) with social information (based on the behavior of other individuals), allowing the group to reach a single collective choice. Previous studies of consensus decision making processes have focused on the informational aspects of behavioral choice, assuming that individuals make choices based solely on their likelihood of being beneficial (e.g., rewarded). However, decisions by both humans and nonhuman animals systematically violate such expectations. Furthermore, the typical experimental paradigm of assessing binary decisions, those between two mutually exclusive options, confounds two aspects common to most group decisions: minimizing uncertainty (through the use of personal and social information) and maintaining group cohesion (for example, to reduce predation risk). Here we experimentally disassociate cohesion-based decisions from information-based decisions using a three-choice paradigm and demonstrate that both factors are crucial to understanding the collective decision making of schooling fish. In addition, we demonstrate how multiple informational dimensions (here color and stripe orientation) are integrated within groups to achieve consensus, even though no individual is explicitly aware of, or has a unique preference for, the consensus option. Balancing of personal information and social cues by individuals in key frontal positions in the group is shown to be essential for such group-level capabilities. Our results demonstrate the importance of integrating informational with other social considerations when explaining the collective capabilities of group-living animals.

Shoaling in zebrafish: what we don’t know

Abstract Zebrafish have been gaining increasing popularity in behavioral neuroscience. However, the number of behavioral test paradigms specifically designed for zebrafish, and in general the amount of information available on the behavior of this species, is relatively small when compared with classical laboratory model organisms such as the mouse, the rat, and the fruit fly. A particularly typical behavioral feature of zebrafish is shoaling, i.e., group formation. Given the importance of social behavior in our own species and the fact that zebrafish possess several characteristics similar to those of other vertebrates, including humans, at many levels of biological organization (e.g., neuroanatomy, neurochemistry, biochemical processes, and amino acid sequence of proteins or nucleotide sequence of genes), the zebrafish is expected to be an excellent tool not only for basic research but perhaps also for translational research. Briefly, we propose that once social behavior of the zebrafish is better characterized and once appropriate behavioral methods have been developed, this species can be utilized for the analysis of the mechanisms of social behavior of other vertebrates including our own. In this review, we discuss general principles of shoaling and highlight what we know and what we do not know about this behavior as it pertains to zebrafish.

Effects of nicotine and alcohol on zebrafish (Danio rerio) shoaling.

The zebrafish has been used in the analysis of the effects of drugs of abuse, including alcohol and nicotine. In the current study, we investigate the effects of these drugs on shoaling, group-forming behavior, in zebrafish, using a newly developed set of behavioral measures. We expose our fish acutely to 0.25, 0.50, 0.75 or 1.00% (% v/v) ethyl alcohol or 4 or 8 mg/L nicotine by immersing the fish in the corresponding solutions. The behavior of the exposed fish is compared to controls in a large (91 cm diameter) circular tank in which shoals of 8 subjects under the same treatment are allowed to swim freely. Several measures of shoaling are quantified including the nearest neighbour distance (NND), inter-individual distance (IID), swimming speed, polarization (a measure of the directional synchronization of the shoal), and the number and duration of excursions (departures from the shoal). Alcohol and nicotine were both found to exert significant effects on shoaling but impaired the behavior in different ways. For example, alcohol strongly disrupted polarization and only modestly reduced shoal cohesion, while nicotine had only a modest effect on polarization but robustly decreased shoal cohesion. Neither drug affected the number or the duration of excursions, but both reduced swimming speed. These results underscore the notion that using multiple measures of social behavior may allow one to characterize and distinguish different aspects of drug effects on behavior, which may facilitate discovery of novel drugs in drug screens and may also be utilized in the analysis of underlying mechanisms.

What-where-when memory in pigeons.

The authors report a novel approach to testing episodic-like memory for single events. Pigeons were trained in separate sessions to match the identity of a sample on a touch screen, to match its location, and to report on the length of the retention interval. When these 3 tasks were mixed randomly within sessions, birds were more than 80% correct on each task. However, performance on 2 different tests in succession after each sample was not consistent with an integrated memory for sample location, time, and identity. Experiment 2 tested binding of location and identity memories in 2 different ways. The results were again consistent with independent feature memories. Implications for tests of episodic-like memory are discussed.

Modeling the effects of enclosure size on geometry learning.

Several recent studies have shown that chickens, fish, and humans trained to find a reward in a corner of a rectangular enclosure with distinctive features rely more on the geometry of the enclosure in small enclosures and rely more on the features in large enclosures. Here, these results are modeled using a recent associative model of geometry learning [Miller, N.Y., Shettleworth, S.J., 2007. Learning about environmental geometry: an associative model. J. Exp. Psychol. Anim. B 33, 191-212]. By adjusting the salience of either geometric or featural information or both the model is capable of reproducing much of the data on the effects of enclosure size on geometry learning.

Redefining membership in animal groups

Groups of animals—flocks, herds, shoals, and swarms—are often dynamical entities. Relative positions of group members change, and most groups divide and re-form on multiple timescales. Few studies, however, have attempted to define when an animal is or is not within a group. Most authors adopt arbitrary distance thresholds, such as the elective group size (EGS), which assume that animals closer than some threshold distance are in the same group. In the present article, we define a group-membership criterion derived from dynamical statistical considerations and based on detailed trajectories of all members of a moving group. We demonstrate the use of our criterion to track the comings and goings in shoals of zebrafish (Danio rerio) and the gradual dissolution of the shoal across multiple exposures to a testing tank. We present a novel measure of group cohesion based on our group membership criterion and demonstrate that excursions away from the shoal explain some previous observations of the dynamics of shoaling. Finally, we show that excursions away from a shoal are accompanied by an increase in swimming speed. Applying similar criteria to data from other species may clarify some of the common features of animal collective motion.

Estimation models describe well collective decisions among three options.

Miller et al. (1) demonstrate, by confronting groups of fish with three options, that information can be effectively integrated, allowing consensus despite no individual being aware of the consensus option. The different ways in which the conflict can be resolved allow testing of collective decision-making theories.