Habituation-like Process Research Articles

Comparing fear responses of two lizard species across habitats varying in human impact

Abstract Animals that are successful in urban habitats often have reduced antipredator responses toward people (sometimes called “fear” responses). However, few studies test whether sympatric species differ in their responses to humans, which may explain differing sensitivities to urbanization. Here, we quantified the behavioral and physiological responses to humans in two lizard species, side-blotched lizards (Uta stansburiana) and western fence lizards (Sceloporus occidentalis), across three different habitat types that vary in human impact: natural habitats with low levels of human activity, natural habitats with high levels of human activity, and urban habitats. We found that side-blotched lizards had longer flight initiation distances, were found closer to a refuge, and were more likely to hide than fence lizards, behaviors that could indicate greater fearfulness. Both lizard species were found closer to a refuge and were also more likely to hide in the urban habitat than in the natural habitat with low human impact, which could represent adaptive behaviors for increased risks in urban areas (e.g. cats). Western fence lizards exhibited lower body sizes and conditions in the habitats with moderate and high levels of human activity, whereas these traits did not differ among habitats in side-blotched lizards. Baseline and stress-induced corticosterone concentrations did not differ across habitats for both species, suggesting that human-impacted habitats were not stressful or that lizards had undergone habituation-like processes in these habitats. Taken together, our results highlight the importance of standardized measurements across multiple species in the same habitats to understand differential responses to human-induced environmental change.

Urban birds become less fearful following COVID-19 reopenings.

Following the COVID-19 pandemic, many people around the world stayed home, drastically altering human activity in cities. This exceptional moment provided researchers the opportunity to test how urban animals respond to human disturbance, in some cases testing fundamental questions on the mechanistic impact of urban behaviours on animal behaviour. However, at the end of this 'anthropause', human activity returned to cities. How might each of these strong shifts affect wildlife in the short and long term? We focused on fear response, a trait essential to tolerating urban life. We measured flight initiation distance-at both individual and population levels-for an urban bird before, during and after the anthropause to examine if birds experienced longer-term changes after a year and a half of lowered human presence. Dark-eyed juncos did not change fear levels during the anthropause, but they became drastically less fearful afterwards. These surprising and counterintuitive findings, made possible by following the behaviour of individuals over time, has led to a novel understanding that fear response can be driven by plasticity, yet not habituation-like processes. The pandemic-caused changes in human activity have shown that there is great complexity in how humans modify a behavioural trait fundamental to urban tolerance in animals.

Beyond Extinction: Prolonged Conditioning and Repeated Threat Exposure Abolish Contextual Renewal of Fear-Potentiated Startle Discrimination but Leave Expectancy Ratings Intact.

Extinction treatments decrease fear via repeated exposures to the conditioned stimulus (CS) and are associated with a return of fear. Alternatively, fear can be reduced via reductions in the perceived intensity of the unconditioned stimulus (US), e.g., through repeated exposures to the US. Promisingly, the few available studies show that repeated US exposures outperform standard extinction. US exposure treatments can decrease fear via two routes: (1) by weakening the CS–US association (extinction-like mechanism), and/or (2) by weakening the subjective US aversiveness (habituation-like mechanism). The current study further investigated the conditions under which US exposure treatment may reduce renewal, by adding a group in which CS–US pairings continued following fear acquisition. During acquisition, participants learned that one of two visual stimuli (CS+/CS−) predicted the occurrence of an aversive electrocutaneous stimulus (US). Next, the background context changed and participants received one of three interventions: repeated CS exposures, (2) repeated US exposures, or (3) continued CS–US pairings. Following repeated CS exposures, test presentations of the CSs in the original conditioning context revealed intact CS+/CS− differentiation in the fear-potentiated startle reflex, while the differentiation was abolished in the other two groups. Differential US expectancy ratings, on the other hand, were intact in all groups. Skin conductance data were inconclusive because standard context renewal following CS exposures did not occur. Unexpectedly, there was no evidence for a habituation-like process having taken place during US exposures or continued CS–US pairings. The results provide further evidence that US exposures outperform the standard extinction treatment and show that effects are similar when US exposures are part of CS–US pairings.

Australian magpies exhibit increased tolerance of aircraft noise on an airport, and are more responsive to take-off than to landing noises

Context On airports, birds often exhibit escape behaviour in response to aircraft. Avian escape behaviours can enable birds to effectively avoid collisions with aircraft, although some are maladaptive and may increase the risk of collision (e.g. erratic flying). Habituation and habituation-like processes among birds potentially mediate the likelihood of aircraft-bird collisions. Moreover, because managers exploit avian escape behaviour to reduce bird–aircraft collision risks, habituation may decrease the efficiency of bird-hazard management. Aims Our aim was to better understand avian behavioural responses to approaching aircraft, which may inform bird-hazard management. Methods We examined the response of Australian magpie, Cracticus tibicen, a species commonly involved in collisions with aircraft, to the noise associated with take-off and landing in three areas: airside, on airport but not airside, and off airport. Key results Magpies responded to aircraft noise in a nuanced way. Take-off produced more responses, and more intense responses, than did landing; both resulted in more frequent, and more intense, responses than did a ‘silent’ control. Responses were least likely, and response latencies were longer, airside, followed by on airport but not airside, and off airport. Intensity of responses was similar across these areas. Conclusions Magpies on the airside were least responsive, and this might influence their strike risk. Implications Given that most wildlife collisions occur during take-off and landing and at low altitudes, and that take-off has greatest overall strike risk, the lack of responsiveness of airside-inhabiting magpies may contribute to collision risk.

Nonassociative learning processes determine expression and extinction of conditioned fear in mice

Freezing to a tone following auditory fear conditioning is commonly considered as a measure of the strength of the tone-shock association. The decrease in freezing on repeated nonreinforced tone presentation following conditioning, in turn, is attributed to the formation of an inhibitory association between tone and shock that leads to a suppression of the expression of fear. This study challenges these concepts for auditory fear conditioning in mice. We show that acquisition of conditioned fear by a few tone-shock pairings is accompanied by a nonassociative sensitization process. As a consequence, the freezing response of conditioned mice seems to be determined by both associative and nonassociative memory components. Our data suggest that the intensity of freezing as a function of footshock intensity is primarily determined by the nonassociative component, whereas the associative component is more or less categorical. We next demonstrate that the decrease in freezing on repeated nonreinforced tone presentation following conditioning shows fundamental properties of habituation. Thus, it might be regarded as a habituation-like process, which abolishes the influence of sensitization on the freezing response to the tone without affecting the expression of the associative memory component. Taken together, this study merges the dual-process theory of habituation with the concept of classical fear conditioning and demonstrates that sensitization and habituation as two nonassociative learning processes may critically determine the expression of conditioned fear in mice.

A Single Exposure to Severe Stressors Causes Long-term Desensitisation of the Physiological Response to the Homotypic Stressor

Although some laboratories have reported that a single session of stress is able to induce a long-lasting sensitisation of the hypothalamic–pituitary–adrenal (HPA) response to further exposures to stress, we have found that a single exposure to severe emotional (immobilisation, restraint or shock) or systemic (endotoxin) stressors reduces the responsiveness of the HPA to the same, but not to a novel (heterotypic), stressor, in which case a slight sensitisation was observed. Long-term desensitisation has been found to reduce not only secretion of peripheral HPA hormones (ACTH and corticosterone), but also to reduce responses of central components of the HPA axis (c-fos and CRF gene expression at the level of the paraventricular nucleus of the hypothalamus, PVN). In addition, desensitisation also applies to the impact of the stressor on food intake and, probably, to stress-induced hyperglycaemia. The development of long-term desensitisation of the HPA axis does not appear to be a universal consequence of exposure to severe stressors as it was not observed in response to insulin-induced hypoglycaemia. Whether or not the development of long-term effects of stress depend on the specific pathways activated by particular stressors remains to be tested. The observed desensitisation of the HPA axis in response to the homotypic stressor shows two special features which makes it difficult to be interpreted in terms of an habituation-like process: (a) the effect increased with time (days to weeks) elapsed between the first and second exposure to the stressor, suggesting a progressive maturational process; and (b) the stronger the stressor the greater the long-term desensitisation. Therefore, it is possible that desensitisation of the HPA axis is the sum of two different phenomena: long-term effects and habituation-like processes. The contribution of the former may be more relevant with severe stressors and longer inter-stress intervals, and that of the latter with mild stressors and repeated exposures. Long-term stress-induced changes may not take place at the level of the PVN itself, but in brain nuclei showing synaptic plasticity and putatively involved in the control of the HPA axis and other physiological responses. As for the precise areas involved, these remain to be characterized.

An investigation of habituation in the jellyfish Aurelia aurita

Three experiments were conducted to examine the effectiveness of different forms of tactile stimulation, probe and stream, and interstimulus intervals (ISI) in producing habituation in the polypoid sessile stage of the jellyfish Aurelia aurita. Results from Experiment 1 showed that polyps significantly decreased their responsiveness to both forms of tactile stimulation with 30-s ISI across 60 trials. Response to a novel stimulus indicated that the response decrement had not been due to fatigue. When the ISI was lengthened to 6 min in Experiment 2, response to the probe form of tactile stimulation did not significantly decrease across 20 trials. Using an ISI of 1 min in Experiment 3, response to the probe form of tactile stimulation decreased significantly across 40 trials. A significant increase in response to the original stimulus (dishabituation) following presentation of a novel stimulus indicated that response decrement was due to habituation or a habituation-like process rather than simple effector fatigue or sensory adaptation.

Habituation in the rat fetus.

Rat fetuses exhibit motor and cardiac responses to chemosensory stimulation on Days 20 and 21 of gestation. The first experiment demonstrated that fetuses exhibit an increase in overall motor activity and decrease in heartrate in response to an initial intraoral infusion of a lemon solution. After a series of nine exposures, however, fetuses no longer exhibit motor or cardiac responses to lemon infusion, suggesting the existence of a habituation-like process. Responsiveness recovers spontaneously following a 3- to 9-min period without stimulation. In a second experiment, a dishabituation treatment was administered to distinguish habituation, which is a centrally mediated decrement in response, from effector fatigue, sensory adaptation, and other peripheral mechanisms that can result in reduced responsiveness. A single infusion of mint following a series of nine lemon exposures was effective in reinstating fetal motor responses to lemon on both Days 20 and 21, but reinstated cardiac responses only on Day 21. Rat fetuses habituate to repeated chemosensory stimulation, suggesting the utility of the habituation paradigm in measuring CNS development during the perinatal period.

The persistence of attack satiation in female golden hamsters

Female hamsters were allowed to attack a series of target hamsters until they reached a criterion of attack satiation. Following delays of 0, 24, or 48 hr they were then presented with a novel “probe” target. Attacks on the probe target were reduced to 26% of baseline at 0 delay and had returned to 71% of baseline by 48 hr. The number of attacks necessary to achieve satiation criterion increased then decreased over the three test occasions, suggesting that habituationlike processes may contribute to, but cannot wholly account for, the satiation effect.

Forebrain monoamines and associative learning: I. Latent inhibition and conditioned inhibition

Two experiments evaluated the effects of depletion of forebrain norepinephrine (NE) or serotonin (5-HT) on two forms of internal inhibition. Experiment 1 examined the role of NE and 5-HT depletion on latent inhibition: rats with dorsal bundle or raphe lesions or vehicle control rats were trained to one of two pre-exposure conditions (single vs multiple stimuli) or to a non-pre-exposure control prior to conditioning. The results of this experiment showed that latent inhibition was attenuated under either condition of pre-exposure following depletion of 5-HT but that attenuation was present in NE depleted rats only when pre-exposed to multiple stimuli. Experiment 2 assessed the rate at which a conditioned inhibitor was established following NE or 5-HT depletion. The results of Experiment 2 indicated that the formation of a conditioned inhibitor was unimpaired following depletion of either NE or 5-HT. The results of Experiment 1 demonstrate that 5-HT and NE have different effects on associative processes: 5-HT apparently affects a habituation-like process, whereas NE is an important influence on more complex mechanisms involving the comparison of new with previously acquired information. The findings of Experiment 2 are consistent with behavioral investigations which show that conditioned inhibition affects output processes rather than the salience of stimuli.