Minimal motifs for habituating systems.

Habituation-a phenomenon in which a dynamical system exhibits a diminishing response to repeated stimulations that eventually recovers when the stimulus is withheld-is universally observed in living systems from animals to unicellular organisms. Despite its prevalence, generic mechanisms for this fundamental form of learning remain poorly defined. Drawing inspiration from prior work on systems that respond adaptively to step inputs, we study habituation from a nonlinear dynamics perspective. This approach enables us to formalize classical hallmarks of habituation that have been experimentally identified in diverse organisms and stimulus scenarios. We use this framework to investigate distinct dynamical circuits capable of habituation. In particular, we show that driven linear dynamics of a memory variable with static nonlinearities acting at the input and output can implement numerous hallmarks in a mathematically interpretable manner. This work establishes a foundation for understanding the dynamical substrates of this primitive learning behavior and offers a blueprint for the identification of habituating circuits in biological systems.

Understanding inter-individual variability of experimental pain habituation and conditioned pain modulation in healthy individuals.

Although reduced experimental pain habituation is proposed as a proxy of diminished endogenous pain modulatory capacity in chronic pain, prior studies show contradictory findings. Even across healthy participants, pain habituation varies substantially, which may relate to another measure of endogenous pain modulation, i.e., conditioned pain modulation (CPM). Hence, this study investigated the relationship between pain habituation and CPM. Pain habituation was assessed in 45 healthy participants between two blocks of 15-20 contact-heat stimuli applied to the hand. Habituation of subjective pain ratings and objective neurophysiological readouts (contact-heat evoked potential (CHEP) and palmar sympathetic skin response (SSR)) was investigated. CPM was assessed by comparing heat pain thresholds before and after hand immersion in a noxious cold (9 °C) and lukewarm water bath (32 °C, to control for repeated measures effects). Pain habituation showed a large variability, with subjective but not objective pain habituation correlating with cold-induced CPM effects (r = 0.50; p = 0.025). This correlation was not observed for 'true' CPM effects (corrected for repeated measures effects) nor for CPM effects induced by a lukewarm water bath. These findings suggest that the observed variability in subjective pain habituation may be influenced by both descending endogenous pain modulation and peripheral adaptation processes associated with repeated measures. Objective pain habituation readouts, i.e., CHEPs and SSRs, capture different, complementary aspects of endogenous pain modulation.

Learning to ignore visual onset distractors hinges on a configuration-dependent coordinates system.

Decrement of attentional capture elicited by visual onset distractors, consistent with habituation, has been extensively characterized over the past several years. However, the type of spatial frame of reference according to which such decrement occurs in the brain remains unknown. Here, four related experiments are reported to shed light on this issue. Observers were asked to discriminate the orientation of a titled line while ignoring a salient but task-irrelevant visual onset that occurred on some trials. The experiments all involved an initial habituation phase, during which capture elicited by the onset distractor progressively decreased, as in prior studies. Importantly, in all experiments, the location of the target and the distractor remained fixed during this phase. After habituation was established, in a final test phase of the various experiments, the spatial arrangement of the target and the distractor was changed to test for the relative contribution to habituation of retinotopic, spatiotopic, and configuration-dependent visual representations. Experiment 1 indicated that spatiotopic representations contribute little, if at all, to the observed decrement in attentional capture. The results from Experiment 2 were compatible with the notion that such capture reduction occurs in either retinotopic- or configuration-specific representations. However, Experiment 3 ruled out the contribution of retinotopic representations, leaving configuration-specific representation as the sole viable interpretation. This conclusion was confirmed by the results of Experiments 4 and 5. In conclusion, visual onset distractors appear to be rejected at a level of the visual hierarchy where visual events are encoded in a configuration-specific or context-dependent manner. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Novel neurophysiological evidence for preserved pain habituation across chronic pain conditions.

OBJECTIVE: The present study aimed to investigate whether subjective and objective measures of pain habituation can be used as potential markers for central sensitization across various chronic pain patients. METHODS: Two blocks of contact-heat stimuli were applied to a non-painful area in 93 chronic pain patients (low back pain, neuropathic pain, and complex regional pain syndrome) and 60 healthy controls (HC). Habituation of pain ratings, contact-heat evoked potentials (CHEP), and sympathetic skin responses (SSR) was measured. RESULTS: There was no significant difference in any measure of pain habituation between patients and HC. Even patients with apparent clinical signs of central sensitization showed no reduced pain habituation. However, prolonged baseline CHEP and SSR latencies (stimulation block 1) were found in patients compared to HC (CHEP: Δ-latency = 23 ms, p = 0.012; SSR: Δ-latency = 100 ms, p = 0.022). CONCLUSION: Given the performed multimodal neurophysiological testing protocol, we provide evidence indicating that pain habituation may be preserved in patients with chronic pain and thereby be of limited use as a sensitive marker for central sensitization. These results are discussed within the framework of the complex interactions between pro- and antinociceptive mechanism as well as methodological issues. The prolonged latencies of CHEP and SSR after stimulation in non-painful areas may indicate subclinical changes in the integrity of thermo-nociceptive afferents, or a shift towards antinociceptive activity. This shift could potentially affect the relay of ascending signals. SIGNIFICANCE: Our findings challenge the prevailing views in the literature and may encourage further investigations into the peripheral and central components of pain habituation, using advanced multimodal neurophysiological techniques.

Protocol to evaluate the effectiveness of a virtual-reality-based behavioral intervention in enhancing sensory responses to real-world warning.

Habituation to signals that warn of a potential danger in high-risk work environments is a critical causal factor of workplace accidents. Such habituation is hard to measure in a real-world setting, and no existing intervention can effectively curb it. Here, we present a protocol to enhance workers' sensory responses to frequently encountered warnings at workplaces using a virtual-reality-based behavioral intervention. We describe steps for performing a virtual reality experiment and an electroencephalography (EEG) experiment with human participants. For complete details on the use and execution of this protocol, please refer to Kim et al.1.

Habituation of Central and Electrodermal Responses to an Auditory Two-Stimulus Oddball Paradigm.

The orienting reaction (OR) towards a new stimulus is subject to habituation, i.e., progressively attenuates with stimulus repetition. The skin conductance responses (SCRs) are known to represent a reliable measure of OR at the peripheral level. Yet, it is still a matter of debate which of the P3 subcomponents is the most likely to represent the central counterpart of the OR. The aim of the present work was to study habituation, recovery, and dishabituation phenomena intrinsic to a two-stimulus auditory oddball paradigm, one of the most-used paradigms both in research and clinic, by simultaneously recording SCRs and P3 in twenty healthy volunteers. Our findings show that the target stimulus was capable of triggering a more marked OR, as indexed by both SCRs and P3, compared to the standard stimulus, that could be due to its affective saliency and relevance for task completion; the application of temporal principal components analysis (PCA) to the P3 complex allowed us to identify several subcomponents including both early and late P3a (eP3a; lP3a), P3b, novelty P3 (nP3), and both a positive and a negative Slow Wave (+SW; -SW). Particularly, lP3a and P3b subcomponents showed a similar behavior to that observed for SCRs , suggesting them as central counterparts of OR. Finally, the P3 evoked by the first standard stimulus after the target showed a significant dishabituation phenomenon which could represent a sign of the local stimulus change. However, it did not reach a sufficient level to trigger an SCR/OR since it did not represent a salient event in the context of the task.

Tropospheric ozone effect on olfactory perception and olfactory bulb dopaminergic interneuron excitability.

Ozone (O3) forms in the Earth's atmosphere, both naturally and by reactions of man-made air pollutants. Deleterious effects of O3 have been found in the respiratory system. Here, we examine whether O3 alters olfactory behavior and cellular properties in the olfactory system. For this purpose, mice were exposed to O3 at a concentration found in highly polluted city air [0.8 ppm], and the behavior elicited by social and non-social odors in habituation/dishabituation tests was assessed. In addition, the electrical responses of dopaminergic olfactory bulb (OB) neurons were also evaluated. O3 differentially compromises olfactory perception to odors: it reduces responses to social and non-social odors in Swiss Webster mice, while this effect was observed in C57BL/6 J mice only for some non-social odors. Additionally, O3 reduced the rate of spontaneous spike firing in periglomerular dopaminergic cells (PG-DA) of the OB. Because this effect could reflect changes in excitability and/or synaptic inputs, the ability of O3 to alter PG-DA spontaneous activity was also tested together with cell membrane resistance, membrane potential, rheobase and chronaxie. Taken together, our data suggest the ability of O3 to affect olfactory perception.

Cognitive asymmetry in rats in response to emergent vs. disappearing affordances.

This study examines the effects of novel environmental changes on the behavior of rats in an experimental chamber. We hypothesized that newly discovered opportunities, detected by the animal's cognitive system, would motivate greater investigation of environmental changes than comparable changes that prevent a given behavior. Three experiments differed in the emergence vs. elimination of affordances represented by open or closed tunnels. In Experiment 1, rats were habituated to a chamber with all four tunnels closed, and then two tunnels were opened. In Experiment 2, rats were habituated to a chamber where all four tunnels were open, and then two tunnels were closed. In Experiment 3, rats were habituated to a chamber with two open tunnels on one side, and two closed tunnels on the other. Then, the arrangement of open and closed tunnels was swapped. Results of the Exp. 1 show that the rats responded by spending more time near the newly opened tunnels and less time near the closed tunnels, the central zone, and the transporter. This suggests that rats are more motivated to investigate the environmental change combined with the emergent affordance (opening of the tunnels) than the environmental change alone. In Exp. 2, the rats responded by spending more time near the open tunnels and less time in the central zone. This suggests that the rats are more triggered by the available affordances (open tunnels) than by the environmental change (closed tunnels). Finally, in Exp. 3, the rats responded by spending more time near the newly opened tunnels and less near the central zone. However, they did not spend less time near the newly closed tunnels. These results suggest that rats process both the novelty itself and the emergence/disappearance of available affordances. The results are discussed regarding the cognitive asymmetry in the perception of emergent vs. disappearing affordances. It is proposed that the rat's cognitive system is specialized for detecting newly emergent environmental opportunities/affordances rather than novelty in general.

Non-dual awareness and sensory processing in meditators: Insights from startle reflex modulation.

Startle modulation paradigms, namely habituation and prepulse inhibition (PPI), can offer insight into the brain's early information processing mechanisms that might be impacted by regular meditation practice. Habituation refers to decreasing response to a repeatedly-presented startle stimulus, reflecting its redundancy. PPI refers to response reduction when a startling stimulus "pulse" is preceded by a weaker sensory stimulus "prepulse" and provides an operational measure of sensorimotor gating. Here, we examined habituation and PPI of the acoustic startle response in regular meditators (n = 32), relative to meditation-naïve individuals (n = 36). Overall, there was no significant difference between meditators and non-meditators in habituation or PPI, but there was significantly greater PPI in meditators who self-reported being able to enter and sustain non-dual awareness during their meditation practice (n = 18) relative to those who could not (n = 14). Together, these findings suggest that subjective differences in meditation experience may be associated with differential sensory processing characteristics in meditators.

Unravelling habituation for COVID-19-related information: A panel data study in Japan.

This study examines people's habituation to COVID-19-related information over almost three years. Using publicly available data from 47 Japanese prefectures, I analyse how human mobility responded to COVID-19-related information, such as the number of COVID-19-infected cases, the declaration of a state of emergency (DSE), and several doses of vaccine using an interactive effects model, which is a type of panel data regression. The results show that Japanese citizens were generally fearful and cautious during the first wave of the unknown infection. As such, a 1% week-on-week increase in the number of infected cases results in a decrease in human mobility by 1.09-percentage-point (pp) week-on-week. However, they gradually became habituated to similar infection information during the subsequent waves, which is reflected in 0.71 pp and 0.29 pp decreases in human mobility in the second and third waves. Nevertheless, the level of habituation decreased in response to the different types of the infection, such as new variants in the fourth wave, with 0.50 pp decrease. By contrast, regarding the DSE, it is more plausible to consider that human mobility responds to varying requests rather than habituate them. Whereas a rapid vaccination program could alleviate people's concerns. I also find spatial spillovers of infection information on human mobility using a spatial weight matrix included in the regression model. However, there is no evidence of DSE or vaccination spatial spillovers, likely because both are valid only in one's own prefecture. The implementation of flexible human mobility control policies by closely monitoring human mobility can prevent excessive or insufficient mobility control requests. Such a flexible policy can efficiently suppress infection spread and prevent economic activity reduction more than necessary. These implications are useful for evidence-based policymaking during future pandemics.

Do sheep (Ovis aries) discriminate human emotional odors?

While sheep can detect and discriminate human emotions through visual and vocal cues, their reaction to human body odors remains unknown. The present study aimed to determine whether sheep (Ovis aries) can detect human odors, olfactorily discriminate stressed from non-stressed individuals, and behave accordingly based on the emotional valence of the odors. Axillary secretions from 34 students were collected following an oral examination (stress odor) or a regular class (non-stress odor). Fourteen female and 15 male lambs were then exposed to these odors through a habituation-dishabituation procedure. The habituation stimulus was presented four times for one minute, followed by the dishabituation stimulus presented once for one minute. Behavioral variables included spatiality relative to target odors, approach/withdrawal, ear positioning, sniffing, ingestion, and vocalization. Both female and male lambs more often positioned their ears backwards/forwards, and asymmetrically when exposed to the dishabituation stimulus, but regardless of their stress or non-stress value. They also changed their approach behavior when exposed to the dishabituation stimuli. Lambs displayed some behavioral signs of discrimination between the habituation and dishabituation odors, but regardless of their relation to stress or non-stress of human donors. In sum, this exploratory study suggests that young sheep respond negatively to the odor of unfamiliar humans, without showing any specific emotional contagion related to the stress odor. This exploratory study suggests young ovines can detect human body odor, a further step toward understanding the human-sheep relationship.

Social participation is associated with a habituated blood pressure response to recurrent stress.

Lower cardiovascular reactivity is a proposed marker of motivational dysregulation and is related to a range of adverse behavioural and health outcomes. Social participation is a form of motivated behaviour and represents the frequency in which an individual engages in social activities. Low social participation has recently been linked to lower cardiovascular responses to acute psychological stress. With recent work emphasizing the importance of assessing adaptation of the cardiovascular response to recurrent stress, the aim of the current study is to build on previous work by examining the relationship between social participation and cardiovascular stress response adaptation. This study utilised data from the Pittsburgh Cold Study 3 (PCS 3). Two hundred and thirteen participants (M = 30.13; SD = 10.85) completed a social participation measure and had their systolic blood pressure (SBP), diastolic blood pressure (DBP) and heart rate (HR) monitored across two separate standardized stress testing sessions. The testing sessions consisted of a 20-minute baseline and a 15-minute stress task. Results indicated that higher levels of social participation were associated with greater blood pressure habituation to recurrent stress, extending previous work identifying that social participation was associated with higher cardiovascular responses to stress. The present study identifies that those reporting greater levels of social participation may show enhanced stress tolerance when exposed to recurrent stress.

Olfactory investigation in the home cage.

We have developed a behavioral paradigm to study volitional olfactory investigation in mice over several months. We placed odor ports in the wall of a standard cage that administer a neutral odorant stimulus when a mouse pokes its nose inside. Even though animals were fed and watered ad libitum, and sampling from the port elicited no outcome other than the delivery of an odor, mice readily sampled these stimuli hundreds of times per day. This self-paced olfactory investigation persisted for weeks with only modest habituation following the first day of exposure to a given set of odorants. If an unexpected odorant stimulus was administered at the port, the sampling rate increased transiently (in the first 20 min) by an order of magnitude and remained higher than baseline throughout the subsequent day, indicating learned implicit knowledge. Thus, this system may be used to study naturalistic olfactory learning over extended time scales outside of conventional task structures.

Phasic Stimulation of Dopaminergic Neurons of the Lateral Substantia Nigra Increases Open Field Exploratory Behaviour and Reduces Habituation Over Time.

Transient nigrostriatal dopaminergic signalling is well known for its role in reinforcement learning and increasingly so for its role in the initiation of voluntary movement. However, how transient bursts of dopamine modulate voluntary movement remains unclear, likely due to the heterogeneity of the nigrostriatal system, the focus of optogenetic studies on locomotion at sub-sec time intervals, and the overlapping roles of phasic dopamine in behaviour and novelty signalling. In this study we investigated how phasic activity in the lateral substantia nigra pars compacta (lateral SNc) over time affects voluntary behaviours during exploration. Using a transgenic mouse model of both sexes expressing channelrhodopsin (ChR2) in dopamine transporter-expressing cells, we stimulated the lateral SNc while mice explored an open field over two consecutive days. We found that phasic activation of the lateral SNc induced an increase in exploratory behaviours including horizontal movement activity, locomotion initiation, and rearing specifically on the first open field exposure, but not on the second day. In addition, stimulated animals did not habituate to the same extent as their ChR2-negative counterparts, as indicated by a lack of decrease in baseline activity. These findings suggest that rather than prompting voluntary movement in general, phasic nigrostriatal dopamine prompts context-appropriate behaviours. In addition, dopamine signalling that modulates movement acts over longer timescales than the transient signal, affecting behaviour even after the signal has ended.

Revisiting perceptual sensitivity to non-native speech in a diverse sample of bilinguals.

Werker and Tees (1984) prompted decades of research attempting to detail the paths infants take towards specialisation for the sounds of their native language(s). Most of this research has examined the trajectories of monolingual children. However, it has also been proposed that bilinguals, who are exposed to greater phonetic variability than monolinguals and must learn the rules of two languages, may remain perceptually open to non-native language sounds later into life than monolinguals. Using a visual habituation paradigm, the current study tests this question by comparing 15- to 18-month-old monolingual and bilingual children's developmental trajectories for non-native phonetic consonant contrast discrimination. A novel approach to the integration of stimulus presentation software with eye-tracking software was validated for objective measurement of infant looking time. The results did not support the hypothesis of a protracted period of sensitivity to non-native phonetic contrasts in bilingual compared to monolingual infants. Implications for diversification of perceptual narrowing research and implementation of increasingly sensitive measures are discussed.

Choline Metabolites Reverse Differentially the Habituation Deficit and Elevated Memory of Tau Null Drosophila.

Impaired neuronal plasticity and cognitive decline are cardinal features of Alzheimer's disease and related Tauopathies. Aberrantly modified Tau protein and neurotransmitter imbalance, predominantly involving acetylcholine, have been linked to these symptoms. In Drosophila, we have shown that dTau loss specifically enhances associative long-term olfactory memory, impairs foot shock habituation, and deregulates proteins involved in the regulation of neurotransmitter levels, particularly acetylcholine. Interestingly, upon choline treatment, the habituation and memory performance of mutants are restored to that of control flies. Based on these surprising results, we decided to use our well-established genetic model to understand how habituation deficits and memory performance correlate with different aspects of choline physiology as an essential component of the neurotransmitter acetylcholine, the lipid phosphatidylcholine, and the osmoregulator betaine. The results revealed that the two observed phenotypes are reversed by different choline metabolites, implying that they are governed by different underlying mechanisms. This work can contribute to a broader knowledge about the physiologic function of Tau, which may be translated into understanding the mechanisms of Tauopathies.

Attentional control influence habituation through modulation of connectivity patterns within the prefrontal cortex: Insights from stereo-EEG.

Attentional control, guided by top-down processes, enables selective focus on pertinent information, while habituation, influenced by bottom-up factors and prior experiences, shapes cognitive responses by emphasizing stimulus relevance. These two fundamental processes collaborate to regulate cognitive behavior, with the prefrontal cortex and its subregions playing a pivotal role. Nevertheless, the intricate neural mechanisms underlying the interaction between attentional control and habituation are still a subject of ongoing exploration. To our knowledge, there is a dearth of comprehensive studies on the functional connectivity between subsystems within the prefrontal cortex during attentional control processes in both primates and humans. Utilizing stereo-electroencephalogram (SEEG) recordings during the Stroop task, we observed top-down dominance effects and corresponding connectivity patterns among the orbitofrontal cortex (OFC), the middle frontal gyrus (MFG), and the inferior frontal gyrus (IFG) during heightened attentional control. These findings highlighting the involvement of OFC in habituation through top-down attention. Our study unveils unique connectivity profiles, shedding light on the neural interplay between top-down and bottom-up attentional control processes, shaping goal-directed attention.

Environmental conditions shape learning in larval zebrafish.

Growing evidence reveals notable phenotypic plasticity in cognition among teleost fishes. One compelling example is the positive impact of enriched environments on learning performance. Most studies on this effect have focused on juvenile or later life stages, potentially overlooking the importance of early life plasticity. To address this gap, we investigated whether cognitive plasticity in response to environmental factors emerges during the larval stage in zebrafish. Our findings indicate that larvae exposed to an enriched environment after hatching exhibited enhanced habituation learning performance compared to their counterparts raised in a barren environment. This work underscores the presence of developmental phenotypic plasticity in cognition among teleost fish, extending its influence to the very earliest stages of an individual's life.

Habituation leads to short but not long term memory formation in mosquito larvae.

In animals, memory allows to remember important locations and conserve energy by not responding to irrelevant stimuli. However, memory formation and maintenance are metabolically costly, making it worthwhile to understand the mechanisms underlying different types of memory and their adaptive value. In this study, we investigated the memory persistence of Aedes aegypti mosquito larvae, after habituation to a visual stimulus. We used an automated tracking system for quantifying the response of mosquito larvae to the passage of a shadow, simulating an approaching predator. First, we compared different retention times, from 4 min to 24 h, and found that mosquito larvae only exhibited memory capabilities less than 3 h after training. Secondly, we investigated the role of inter-trial intervals in memory formation. In contrast to other aquatic invertebrates, mosquito larvae showed no long-term memory even at long inter-trial intervals (i.e., 5 min and 10 min). Our results are discussed in relation to the ecological constraints.

The antipsychotic agent sulpiride microinjected into the ventral pallidum restores positive symptom-like habituation disturbance in MAM-E17 schizophrenia model rats.

Dysfunction of subcortical D2-like dopamine receptors (D2Rs) can lead to positive symptoms of schizophrenia, and their analog, the increased locomotor activity in schizophrenia model MAM-E17 rats. The ventral pallidum (VP) is a limbic structure containing D2Rs. The D2R antagonist sulpiride is a widespread antipsychotic drug, which can alleviate positive symptoms in human patients. However, it is still not known how sulpiride can influence positive symptoms via VP D2Rs. We hypothesize that the microinjection of sulpiride into the VP can normalize hyperactivity in MAM-E17 rats. In addition, recently, we showed that the microinjection of sulpirid into the VP induces place preference in neurotypical rats. Thus, we aimed to test whether intra-VP sulpiride can also have a rewarding effect in MAM-E17 rats. Therefore, open field-based conditioned place preference (CPP) test was applied in neurotypical (SAL-E17) and MAM-E17 schizophrenia model rats to test locomotor activity and the potential locomotor-reducing and rewarding effects of sulpiride. Sulpiride was microinjected bilaterally in three different doses into the VP, and the controls received only vehicle. The results of the present study demonstrated that the increased locomotor activity of the MAM-E17 rats was caused by habituation disturbance. Accordingly, larger doses of sulpiride in the VP reduce the positive symptom-analog habituation disturbance of the MAM-E17 animals. Furthermore, we showed that the largest dose of sulpiride administered into the VP induced CPP in the SAL-E17 animals but not in the MAM-E17 animals. These findings revealed that VP D2Rs play an important role in the formation of positive symptom-like habituation disturbances in MAM-E17 rats.