Easy to process, hard to control: Transient and sustained processing fluency impairs cognitive control adjustments to conflict.

Recent research suggests that the cognitive monitoring system of control could be using negative affective cues intrinsic to changes in information processing to initiate top-down regulatory mechanisms. Here, we propose that positive feelings of ease-of-processing could be picked up by the monitoring system as a cue indicating that control is not necessary, leading to maladaptive control adjustments. We simultaneously target control adjustments driven by task context and on a trial-by-trial level, macro-, and micro-adjustments. This hypothesis was tested using a Stroop-like task comprised trials varying in congruence and perceptual fluency. A pseudo randomisation procedure within different proportion of congruence conditions was used to maximise discrepancy and fluency effects. Results suggest that in a mostly congruent context participants committed more fast errors when incongruent trials were easy-to-read. Moreover, within the mostly incongruent condition, we also found more errors on incongruent trials after experiencing the facilitation effect of repeated congruent trials. These results suggest that transient and sustained feelings of processing fluency can downregulate control mechanisms, leading to failed adaptive adjustments to conflict.

Bad after bad is good: previous trial disfluency reduces interference promoted by incongruence.

Conflict and perceptual disfluency have been shown to lead to adaptive, sequential, control adjustments. Here, we propose that these effects can be additive, suggesting their integration into a general feeling of disfluent information processing. This hypothesis was tested using an interference task that dynamically mixed trials varying in legibility and/or congruence. Moreover, the manipulation of the proportion of congruent trials within the task allowed differentiating conditions in which these experiences of fluency may vary. Results showed that progressive increases in processing disfluency elicited a matching decrease in the interference of incongruent fluent trials. This linear effect was significant for all proportion of congruence conditions, although lower when incongruent trials were more frequent. These results highlight the role of feelings in the initiation of control and suggest that the monitoring system could be using changes in information processing fluency as a need-for-control signal.

Stressor controllability modulates the stress response in fish.

BACKGROUND: In humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax). RESULTS: Fish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used. CONCLUSIONS: These results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).

Fighting Assessment Triggers Rapid Changes in Activity of the Brain Social Decision-Making Network of Cichlid Fish.

Social living animals have to adjust their behavior to rapid changes in the social environment. It has been hypothesized that the expression of social behavior is better explained by the activity pattern of a diffuse social decision-making network (SDMN) in the brain than by the activity of a single brain region. In this study, we tested the hypothesis that it is the assessment that individuals make of the outcome of the fights, rather than the expression of aggressive behavior per se, that triggers changes in the pattern of activation of the SDMN which are reflected in socially driven behavioral profiles (e.g., dominant vs. subordinate specific behaviors). For this purpose, we manipulated the perception of the outcome of an agonistic interaction in an African cichlid fish (Oreochromis mossambicus) and assessed if either the perception of outcome or fighting by itself was sufficient to trigger rapid changes in the activity of the SDMN. We have used the expression of immediate early genes (c-fos and egr-1) as a proxy to measure the neuronal activity in the brain. Fish fought their own image on a mirror for 15 min after which they were allocated to one of three conditions for the two last minutes of the trial: (1) they remained fighting the mirror image (no outcome treatment); (2) the mirror was lifted and a dominant male that had just won a fight was presented behind a transparent partition (perception of defeat treatment); and (3) the mirror was lifted and a subordinate male that had just lost a fight was presented behind a transparent partition (perception of victory treatment). Results show that these short-term social interactions elicit distinct patterns in the SDMN and that the perception of the outcome was not a necessary condition to trigger a SDMN response as evidenced in the second treatment (perception of defeat treatment). We suggest that the mutual assessment of relative fighting behavior drives these acute changes in the state of the SDMN.

Audience Effects in Territorial Defense of Male Cichlid Fish Are Associated with Differential Patterns of Activation of the Brain Social Decision-Making Network.

Animals communicate by exchanging signals frequently in the proximity of other conspecifics that may detect and intercept signals not directed to them. There is evidence that the presence of these bystanders modulates the signaling behavior of interacting individuals, a phenomenon that has been named audience effect. Research on the audience effect has predominantly focused on its function rather than on its proximate mechanisms. Here, we have investigated the physiological and neuromolecular correlates of the audience effect in a cichlid fish (Mozambique tilapia, Oreochromis mossambicus). A male was exposed to a territorial intrusion in the presence or absence of a female audience. Results showed that the presence of the female audience increased territorial defense, but elicited a lower androgen and cortisol response to the territorial intrusion. Furthermore, analysis of the expression of immediate early genes, used as markers of neuronal activity, in brain areas belonging to the social decision-making network (SDMN) revealed different patterns of network activity and connectivity across the different social contexts (i.e., audience × intrusion). Overall, these results suggest that socially driven plasticity in the expression of territorial behavior is accommodated in the central nervous system by rapid changes in functional connectivity between nodes of relevant networks (SDMN) rather than by localized changes of activity in specific brain nuclei.

Dear Enemies Elicit Lower Androgen Responses to Territorial Challenges than Unfamiliar Intruders in a Cichlid Fish.

In many territorial species androgen hormones are known to increase in response to territorial intrusions as a way to adjust the expression of androgen-dependent behaviour to social challenges. The dear enemy effect has also been described in territorial species and posits that resident individuals show a more aggressive response to intrusions by strangers than by other territorial neighbours. Therefore, we hypothesized that the dear enemy effect may also modulate the androgen response to a territorial intrusion. Here we tested this hypothesis in male cichlid fish (Mozambique tilapia, Oreochromis mossambicus) using a paradigm of four repeated territorial intrusions, either by the same neighbour or by four different unfamiliar intruders. Neighbour intruders elicited lower aggression and a weaker androgen response than strangers on the first intrusion of the experiment. With repeated intrusions, the agonistic behaviour of the resident males against familiar intruders was similar to that displayed towards strangers. By the fourth intrusion the androgen response was significantly reduced and there was no longer a difference between the responses to the two types of intruders. These results suggest that the dear enemy effect modulates the androgen response to territorial intrusions and that repeated intrusions lead to a habituation of the androgen response.

Linking appraisal to behavioral flexibility in animals: implications for stress research.

In fluctuating environments, organisms require mechanisms enabling the rapid expression of context-dependent behaviors. Here, we approach behavioral flexibility from a perspective rooted in appraisal theory, aiming to provide a better understanding on how animals adjust their internal state to environmental context. Appraisal has been defined as a multi-component and interactive process between the individual and the environment, in which the individual must evaluate the significance of a stimulus to generate an adaptive response. Within this framework, we review and reframe the existing evidence for the appraisal components in animal literature, in an attempt to reveal the common ground of appraisal mechanisms between species. Furthermore, cognitive biases may occur in the appraisal of ambiguous stimuli. These biases may be interpreted either as states open to environmental modulation or as long-lasting phenotypic traits. Finally, we discuss the implications of cognitive bias for stress research.

Testosterone response to competition in males is unrelated to opponent familiarity or threat appraisal.

It has been proposed in the literature that the testosterone (T) response to competition in humans may be modulated by cognitive variables. In a previous experiment with a female sample we have reported that opponent familiarity and threat appraisal moderated the T response to competition in women. With this experiment we aim to investigate if these variables have the same impact on males T response to competition, extending the previous findings in our lab. Forty male participants (20 dyads) were recruited to engage in a same sex, face to face competition using the Number Tracking Test as a competitive task. Levels of T, cortisol (C) and dehydroepiandrosterone (DHEA) were measured before and 20 min after the competition. Results show that losers report higher levels of threat than winners and increased their T levels after the competition, however this T change was not predicted by opponent familiarity or threat appraisal. No variation was detected for C and DHEA levels. These findings suggest that there could be sex differences for the moderators/mediators of the T response to competition in humans.

Androgen modulation of social decision-making mechanisms in the brain: an integrative and embodied perspective.

Apart from their role in reproduction androgens also respond to social challenges and this response has been seen as a way to regulate the expression of behavior according to the perceived social environment (Challenge hypothesis, Wingfield et al., 1990). This hypothesis implies that social decision-making mechanisms localized in the central nervous system (CNS) are open to the influence of peripheral hormones that ultimately are under the control of the CNS through the hypothalamic-pituitary-gonadal axis. Therefore, two puzzling questions emerge at two different levels of biological analysis: (1) Why does the brain, which perceives the social environment and regulates androgen production in the gonad, need feedback information from the gonad to adjust its social decision-making processes? (2) How does the brain regulate gonadal androgen responses to social challenges and how do these feedback into the brain? In this paper, we will address these two questions using the integrative approach proposed by Niko Tinbergen, who proposed that a full understanding of behavior requires its analysis at both proximate (physiology, ontogeny) and ultimate (ecology, evolution) levels.

Threat perception and familiarity moderate the androgen response to competition in women.

Social interactions elicit androgen responses whose function has been posited to be the adjustment of androgen-dependent behaviors to social context. The activation of this androgen response is known to be mediated and moderated by psychological factors. In this study we tested the hypothesis that the testosterone (T) changes after a competition are not simply related to its outcome, but rather to the way the subject evaluates the event. In particular we tested two evaluative dimensions of a social interaction: familiarity with the opponent and the subjective evaluation of the outcome as threat or challenge. Challenge/threat occurs in goal relevant situations and represent different motivational states arising from the individuals' subjective evaluation of the interplay between the task demands and coping resources possessed. For challenge the coping resources exceed the task demands, while threat represents a state where coping resources are insufficient to meet the task demands. In this experiment women competed in pairs, against a same sex opponent using the number tracking test as a competitive task. Losers appraised the competition outcome as more threatening than winners, and displayed higher post-competition T levels than winners. No differences were found either for cortisol (C) or for dehydroepiandrosterone. Threat, familiarity with the opponent and T response were associated only in the loser condition. Moderation analysis suggests that for the women that lost the competition the effect of threat on T is moderated by familiarity with the opponent.