Tricia S. Clement

Fish can infer social rank by observation alone

Transitive inference (TI) involves using known relationships to deduce unknown ones (for example, using A > B and B > C to infer A > C), and is thus essential to logical reasoning. First described as a developmental milestone in children, TI has since been reported in nonhuman primates, rats and birds. Still, how animals acquire and represent transitive relationships and why such abilities might have evolved remain open problems. Here we show that male fish (Astatotilapia burtoni) can successfully make inferences on a hierarchy implied by pairwise fights between rival males. These fish learned the implied hierarchy vicariously (as ‘bystanders’), by watching fights between rivals arranged around them in separate tank units. Our findings show that fish use TI when trained on socially relevant stimuli, and that they can make such inferences by using indirect information alone. Further, these bystanders seem to have both spatial and featural representations related to rival abilities, which they can use to make correct inferences depending on what kind of information is available to them. Beyond extending TI to fish and experimentally demonstrating indirect TI learning in animals, these results indicate that a universal mechanism underlying TI is unlikely. Rather, animals probably use multiple domain-specific representations adapted to different social and ecological pressures that they encounter during the course of their natural lives.

Episodic-like memory in pigeons

It has been proposed that memory for personal experiences (episodic memory, rather than semantic memory) relies on the conscious review of past experience and thus is unique to humans. In an attempt to demonstrate episodic-like memory in animals, we first trained pigeons to respond to the (nonverbal) question “Did you just peck or did you just refrain from pecking?” by training them on a symbolic matching task with differential responding required to the two line-orientation samples and reinforcing the choice of a red comparison if they had pecked and the choice of a green comparison if they had not pecked. Then, in Experiment 1, after providing the conditions for (but not requiring) the pigeons to peck at one new stimulus (a yellow hue) but not at another (a blue hue), we tested them with the new hue stimuli and the red and green comparisons. In Experiment 2, we tested the pigeons with novel stimuli (a circle, which they spontaneously pecked, and a dark response key, which they did not peck) and the red and green comparisons. In both experiments, pigeons chose the comparison appropriate to the response made to the test stimulus. Thus, the pigeons demonstrated that they could remember specific details about their past experiences, a result consistent with the notion that they have the capacity for forming episodic-like memories.

“work ethic” in pigeons: Reward value is directly related to the effort or time required to obtain the reward

Stimuli associated with less effort or with shorter delays to reinforcement are generally preferred over those associated with greater effort or longer delays to reinforcement. However, the opposite appears to be true of stimuli thatfollow greater effort or longer delays. In training, a simple simultaneous discrimination followed a single peck to an initial stimulus (S+FR1 S−FR1) and a different simple simultaneous discrimination followed 20 pecks to the initial stimulus (S+FR20 S−FR20). On test trials, pigeons preferred S+FR20 over S+FR1 and S−FR20 over S−FR1. These data support the view that the state of the animal immediately prior to presentation of the discrimination affects the value of the reinforcement that follows it. This contrast effect is analogous to effects that when they occur in humans have been attributed to more complex cognitive and social factors.

Androgen level and male social status in the African cichlid, Astatotilapia burtoni.

In vertebrates, circulating androgen levels are regulated by the hypothalamic-pituitary-gonadal (HPG) axis through which the brain controls the gonads via the pituitary. Androgen levels ultimately depend on factors including season, temperature, social circumstance, age, and other variables related to reproductive capacity and opportunity. Previous studies with an African cichlid fish, Astatotilapia burtoni, suggested that changes in both testosterone and 11-ketotestosterone (11-KT), an androgen specific to teleost fish, depend on male social status. Here we characterize circulating plasma concentrations of testosterone and 11-KT in socially dominant (territorial) and socially subordinate (non-territorial) males. Territorial males have significantly higher circulating levels of both forms of androgen, which is another defining difference between dominant and subordinate males in this species. These results underscore how internal and external cues related to reproduction are integrated at the level of the HPG axis.

Behavioral coping strategies in a cichlid fish: the role of social status and acute stress response in direct and displaced aggression.

The African cichlid fish, Astatotilapia burtoni, has a complex social system with a sophisticated social hierarchy that offers unique opportunities to understand how social rank and its physiological substrates relate to behavioral strategies. In A. burtoni, a small fraction of the males are dominant (T, territorial), as distinguished by being large, brightly colored, reproductively active, and aggressively defending territories. In contrast, the majority of males are non-dominant (NT, non-territorial), being smaller, drably colored, sexually immature, and typically schooling with females. The social system is regulated by aggressive interactions between males and behavioral responses to aggression can be direct or displaced with respect to the animal that acts. To determine whether direct and displaced behaviors are differentially exhibited by T and NT males, individuals were shown a video presentation of a dominant male displaying aggressively. Analysis of aggressive acts toward the video display and displaced activity toward a tank mate revealed that T males exhibited more direct behavior (toward the video display), while NT males engaged in more displaced behavior (toward tank mates). Because similar experiments with primates suggest that shifts in behavioral strategies are linked to changes in the stress response (as measured by circulating cortisol levels), we measured cortisol levels of T and NT males following exposure to the aggressive stimulus. Although in some animals subordinate males are reported to have higher cortisol levels, here we show that in A. burtoni the endocrine response to specific situations can vary considerably even among animals of the same status. Interestingly, NT males with intermediate cortisol levels showed more directed behavior while NT males with both high and low cortisol levels showed more displaced. This suggests an optimal physiological stress response in NT males that predisposes them to challenge aggressors perhaps making it more likely for them to ascend in status.

Second-order contrast based on the expectation of effort and reinforcement.

Pigeons prefer signals for reinforcement that require greater effort (or time) to obtain over those that require less effort to obtain (T. S. Clement, J. Feltus, D. H. Kaiser, & T. R. Zentall, 2000). Preference was attributed to contrast (or to the relatively greater improvement in conditions) produced by the appearance of the signal when it was preceded by greater effort. In Experiment 1, the authors of the present study demonstrated that the expectation of greater effort was sufficient to produce such a preference (a second-order contrast effect). In Experiments 2 and 3, low versus high probability of reinforcement was substituted for high versus low effort, respectively, with similar results. In Experiment 3, the authors found that the stimulus preference could be attributed to positive contrast (when the discriminative stimuli represented an improvement in the probability of reinforcement) and perhaps also negative contrast (when the discriminative stimuli represented reduction in the probability of reinforcement).

Pigeons group time intervals according to their relative duration.

In the present research, we asked whether pigeons tended to judge time intervals not only in terms of their absolute value but also relative to a duration from which they must be discriminated (i.e., longer or shorter). Pigeons were trained on two independent temporal discriminations. In one discrimination, sample durations of 2 and 8 sec were associated with, for example, red and green hue comparisons, respectively, and in the other discrimination, sample durations of 4 and 16 sec were associated with vertical and horizontal line comparisons, respectively. If pigeons are trained on a temporal discrimination and tested with intermediate durations, the subjective midpoint typically occurs close to the geometric mean of the two trained values. The 4- and 8-sec values were selected to be the geometric mean of the two values in the other discrimination. When a 4-sec test sample was presented with the comparisons from the 2- and 8-sec discrimination, the pigeons preferred the comparison associated with the shorter sample. Similarly, when an 8-sec test sample was presented with the comparisons from the 4-and 16-sec discrimination, the pigeons preferred the comparison associated with the longer sample. Thus, a relative grouping effect was found. That is, durations that should have produced indifferent choice were influenced by their relative durations (shorter than or longer than the alternative) during training.

Choice based on exclusion in pigeons

When humans acquire a conditional discrimination and are given a novel-sample-comparison choice, they often reject a comparison known to be associated with a different sample and choose the alternative comparison by default (or by exclusion). In Experiment 1, we found that if, following matching training, we replaced both of the samples, acquisition took five times longer than if we replaced only one of the samples. Apparently, the opportunity to reject one of the comparisons facilitated the association of the other sample with the remaining comparison. In Experiment 2, we first trained pigeons to treat two samples differently (to associate Sample A with Comparison 1 and Sample B with Comparison 2) and then trained them to associate one of those samples with a new comparison (e.g., Sample A with Comparison 3) and to associate a novel sample (Sample C) with a different, new comparison (Comparison 4). When Sample B then replaced Sample C, the pigeons showed a significant tendency to choose Comparison 4 over Comparison 3. Thus, when given the opportunity, pigeons will choose by exclusion.

Discriminative stimuli that follow the absence of reinforcement are preferred by pigeons over those that follow reinforcement.

Clement, Feltus, Kaiser, and Zentall (2000) found that when pigeons have to work to obtain a discriminative stimulus that is followed by reinforcement, they prefer a discriminative stimulus that requires greater effort over one that requires less effort. The authors suggested that such a preference results from the greater change in hedonic value that occurs between the more aversive event and the onset of the stimulus that signals reinforcement, a contrast effect. It was hypothesized that any stimulus that follows a relatively more aversive event would be preferred over a stimulus that follows a relatively less aversive event. In the present experiment, the authors tested the counterintuitive prediction of that theory, that pigeons should prefer a discriminative stimulus that follows the absence of reinforcement over a discriminative stimulus that follows reinforcement. Results supported the theory.

Development of a Single-Code/Default Coding Strategy in Pigeons

We tested the hypothesis that pigeons could use a cognitively efficient coding strategy by training them on a conditional discrimination (delayed symbolic matching) in which one alternative was correct following the presentation of one sample (one-to-one), whereas the other alternative was correct following the presentation of any one of four other samples (many-to-one). When retention intervals of different durations were inserted between the offset of the sample and the onset of the choice stimuli, divergent retention functions were found. With increasing retention interval, matching accuracy on trials involving any of the many-to-one samples was increasingly better than matching accuracy on trials involving the one-to-one sample. Furthermore, following this test, pigeons treated a novel sample as if it had been one of the many-to-one samples. The data suggest that rather than learning each of the five sample-comparison associations independently, the pigeons developed a cognitively efficient single-code/default coding strategy.