Behavioral Management for Managing Stressors in Primates: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Beatrix Zheng and Version 3 by Beatrix Zheng.

Primates involved in biomedical research experience stressors related to captivity, close contact with caregivers, and may be exposed to various medical procedures while modeling clinical disease or interventions under study. Behavioral management is used to promote behavioral flexibility in less complex captive environments and train coping skills to reduce stress. How animals perceive their environment and interactions is the basis of subjective experience and has a major impact on welfare. Certain traits, such as temperament and species, can affect behavioral plasticity and learning.

  • training
  • nonhuman primates
  • coping
  • temperament
  • behavior
  • welfare

1. Introduction

The ability to effectively cope with stressful situations has a major impact on physical and psychological wellbeing in both animals and humans. Coping consists of strategies and behaviors used to manage situations that are perceived as stressful, divided into two types, positive (e.g., creation of a favorable association or reappraisal) or negative (e.g., avoidance and escape) [1]. Chronic, uncontrolled stress in the absence of effective coping has been associated with an increased risk of developing anxiety, depression, and a range of other disorders [2][3][4]. In the healthcare setting, anxiety or depression, as well as overall patient dissatisfaction, can increase the likelihood of poor compliance with drug or treatment regimens, negatively impacting a variety of patient health outcomes [5][6]. In contrast, positive coping has the potential to reduce distress associated with illness and aversive medical interventions to the extent that effective coping strategies have been shown to improve patient quality of life (QOL) as well as decrease morbidity and mortality [7][8][9][10][11]. A combination of appropriate cognitive and behavioral responses is necessary in order to reinterpret, or blunt, aversive events or demands imposed by stressors and effectively cope [12][13]. Animals involved in biomedical research are intended to closely model diseases and therapies under investigation, which not only exposes them to similar stressors that affect patient quality of life (i.e., inherently imposed by a specific disease state and its intensive medical management) but also those related to the introduction of frequent research interventions in a captive environment. Even with the most skilled care and appropriate pain management, if animals are not adequately prepared these interventions can be perceived as unpredictable and uncontrollable. As a result, interactions with an aversive stimulus can have a variety of behavioral consequences including conditioned anxiety, attempts to avoid or escape treatment, or direct aggression towards caregivers. The frequency of medical intervention can intensify distress as animals do not necessarily habituate to aversive procedures simply through repetition alone. Ultimately, the ability to cope with these stressors impacts animal welfare and scientific outcome parameters [14][15][16][17][18].
In the captive setting, behavioral management is a comprehensive approach combining enrichment, sociality, and training to enhance welfare and foster positive coping [19]. Operant conditioning is an important and frequently used tool in learning and behavioral modification for both routine situations and stressful situations where avoidance learning can lead to maladaptive coping. In the research setting, a number of benefits have been observed in animal models trained to cooperate with their own care, including safer animal-caregiver interactions, improved model validity from reduced levels of outcome-confounding stress, and enhanced welfare [20][21][22][23][24]. Likewise, in pediatric patients, the use of behavioral management techniques that incorporate the opportunity to express choice successfully fosters beneficial cooperative behavior during aversive treatments, highlighting the translational relevance of these paradigms [25][26].
The success of any training paradigm is dependent on the acquisition of specific skills and the speed, or efficiency, of learning. Positive reinforcement training (PRT), defined as ‘adding’ a rewarding stimulus (e.g., preference food item, toys, positive social interaction) upon performance of a desired behavior, is generally considered the ideal training approach [21]. However, PRT alone has been shown to be less effective for training behaviors that have mildly aversive outcomes (e.g., pain from a blood collection or drug injection) and require animals to make a value assessment of whether a reward is ‘worth it’ [27][28]. Though the connection is not well understood, prior research has suggested that temperament is correlated with successful training of simple tasks and can influence an individual’s relative predilection for appetitive versus defensive (e.g., avoidance) motivators, affecting eventual cost–benefit decisions and the overall efficacy of PRT-alone training paradigms [29][30]. Primates with more inhibited temperaments, with behavioral tendencies towards withdrawal or apprehension of the unfamiliar [31], have been shown to have a more difficult time learning simple tasks under a PRT-only paradigm compared to primates with exploratory temperaments, suggesting that inhibited animals may place a greater value on avoidance over reward [32]. When PRT alone is ineffective in suppressing avoidance motivated behavior, a concurrent negative reinforcement training (NRT) component, usually a mild unwanted condition (e.g., reduced working space, elimination of additional sessions when animals accomplish behaviors to promote productivity), can be used intentionally and selectively (as opposed to accidentally) because of the inherent aversive stimuli occurring in most medical situations [33]. Giving animals the opportunity to rehearse the behavior necessary for cooperation or coping with procedures in stepwise in a highly controlled safe environment alters experience from an undesirable one to a tolerable or even a sought after experience when effectively converted to reward seeking. This strategy, desensitization, increases familiarity with a task, while reducing fear, to help decrease overall stress related to the task and can foster the expression of choice and cooperative behavior, indicators of successful coping, in future instances of the task [21][34][35].
Coping has also been linked with temperament, or personality [36][37]. Temperament encompasses the consistent emotional and behavioral traits of an individual that are a major factor influencing the subjective environmental experience [38][39][40][41][42]. The dimensions of temperament and personality are remarkably similar across species [43][44]. Rodent temperament has been used to predict anxiety traits and evaluate physiological mechanisms related to psychopathology [45][46][47][48], while nonhuman primate (NHP) behavior, social constructs, cognitive function, and temperament-defining traits are each closely related to those of humans [49][50][51][52][53]. Temperament influences reactivity to acute and chronic stress, manifesting as changes in physiological parameters such as heart rate, blood pressure, and endocrine response [54][55][56], and has been associated with overall response to stressful clinical situation [38][57]. Since temperament and personality influence how individuals perceive their environment and cope with its stressors, there is likely a similar influence on individual responses to targeted interventions aimed at improving coping and fostering resilience [29][36][37][58][59][60], including various behavioral training paradigms [36]. Temperament has been shown to indirectly influence learning by affecting motivation and preference in learning styles [61][62][63][64]. As such, mixed reinforcement paradigms may have the considerable advantage of motivation across temperament to support wider-spread acquisition of positive coping across all temperament types [65][66][67].
While training animals for cooperation in biomedical research is becoming more common, few studies have examined factors that might influence the success of such behavioral management programs. Using the well-established training program designed to foster NHP cooperation with a variety of research and medical interventions, the reseachers evaluated the influence of individual characteristics such as temperament and species on training outcomes and the acquisition of important coping skills [20]. This retrospective cohort research assessed training success in male and female rhesus (Macaca mulatta) and cynomolgus macaques (Macaca fascicularis) with inhibited and exploratory temperaments. Animals were trained using a standardized mixed reinforcement paradigm [68] to cooperatively present a limb to a caregiver in their familiar home enclosure for the performance of a variety of medically relevant manipulations. While holding environmental and social conditions constant, the researchers probed the influence of temperament, species, sex, and age on the time required for animals to acquire the targeted skills. The researchers defined success as full cooperation with caregivers with the target task, suggestive of a motivational preference towards appetitive, rewarding stimuli relative to avoidance. In human patients, behavioral engagement, active and voluntary participation, and the need for restraint (or lack thereof) have similarly been used to assess coping in the context of medical-related stimuli in human patients [66][69][70]. Similarly, the researchers considered engagement and voluntary participation with direct human contact and medical stimuli indicative of positive coping. There is important translational relevance in this work, especially in pediatrics, where reactivity in children is particularly closely tied to temperament due to developmentally primitive coping mechanisms [71][72]. This research evaluated the relationship between temperament, species, and other demographic variables and the acquisition of coping skills with the aim to both improving captive animal management practices and also reveal novel insights into the interplay between temperament and coping that can inform strategies in the clinic [73][74].

2. Training Differences by Species

Interestingly, the researchers observed significantly different time requirements to complete the same training paradigm between cynomolgus and rhesus macaques suggests there are inherent learning differences and motivational preferences between species [75][76], although the basis for this has yet to be defined. However, this difference of 3 h versus 5 h average total training time in rhesus and cynomolgus macaques, respectively, has little clinical relevance; this is a modest difference in investment in time to train behaviors that will be used in the majority of animals for years. Notwithstanding, understanding the average time commitment required for training a certain animal could have practical implications for study planning related to time management and budgeting. Knowledge of these behavioral differences could prove to be valuable in guiding future model selection, in addition to shaping effective behavioral management practices. From the scientific perspective, deeper understanding of differences in learning behavior influences preclinical model selection to ensure members of the selected species are able to demonstrate the capacity to cooperate, cope, and comply with study procedures in ways that more closely represent the clinical situation. Overall, advancements in the researchers' understanding of species-specific differences in training ability can help improve accuracy of study timeline planning, and improve animal welfare by increasing understanding of what is necessary in order to prepare animals to acquire the coping skills necessary to flourish in the research environment.

3. Temperament and Behavioral Motivations

The researchers also focused on the interaction between temperament and skills acquisition since behavioral inhibition is associated with an increased risk for stress, and subsequently, anxiety and depression [2][8][9][41][42]. Behaviorally inhibited primates were significantly less likely to accept treats from novel handlers, consistent with vigilance, neophobia, and avoidant tendencies during unfamiliar situations. These results agree with previous research showing that inhibited primates are less likely to directly take treats, and further support the use of the human intruder test to accurately assess temperament [20]. Training can support cognitive processes capable of moderating negative reactivity or modulate fearful reactions to allow instead for engagement with frequent, rewarding, and successful interactions, an adaptation consistent with positive coping that decreases stress. In this research, behaviorally inhibited NHPs successfully performed target behaviors at the same rate as those that were more exploratory, suggesting the early-phase mixed reinforcement used in the researchers' program is useful to support skill acquisition and positive coping mechanisms in animals that display high levels of reactivity and distress to novel or unfamiliar objects or people.
Temperament-associated differences in willingness to accept highly palatable treats or other appetitive rewards has important implications related to motivational preferences, which can help inform the design of the most suitable training paradigm for a given animal (e.g., PRT only vs. mixed reinforcement). Previous studies have shown that inhibited primates are significantly less successful in training with a PRT-only based approach, which might be explained by lower motivation to accept positive reinforcers, such as high-valued treats, by behaviorally inhibited animals relative to their more exploratory counterparts [20]. For these inhibited animals that exhibit more fearful, avoidant, hesitant, and relatively neophobic behaviors, the appeal of removing (NR) something unwanted may initially be more motivational than appetitive (PR) rewards [77]. When an unwanted stimulus or condition is subtracted (NR), these animals experience relief, a powerful reinforcer, and trust can be built on the understanding that the trained interaction is safe. When combined sparingly with PRT, NRT can be used to improve training efficacy to reinforce that all interactions with trainers end in a favorable outcome for an animal [68][78][79]. The researchers show that although inhibited animals were less likely to take treats at the initiation of training, they were accepting treats comparably to exploratory animals by the end of the P-Phase of training. Using P-phase as an easy learning phase to modulate reactive tendencies and instead engage animals with frequent rewarding appeared to effectively diminish the effects of temperament in future phases, evident by the absence of significant difference in the time required to complete subsequent training phases. It should be highlighted that during Phase-1 and -2 training, primates were offered a high valued “jackpot” at the end of each training session to offset potential training-related anxiety, foster a positive association with training. Affective state-based cognitive biases can occur when there is no way to buffer or counter-condition a stressful event, and post-training high value rewards can help provide this buffer [80]. It is important to note that even the more inhibited animals were able to benefit from the “jackpot” reward strategy owing to the coping skills and willingness to accept appetitive reinforcers developed during the P-Phase of training and the mixed reinforcement-based training paradigm. These findings suggest that the mixed reinforcement training model, with the incorporation of appropriate familiarization and desensitization steps (in the form of the P-Phase here), supports the learning and development of improved coping strategies required for training success in both exploratory animals, and notably, inhibited animals. The combination of push–pull motivators utilized by mixed-reinforcement may be more effective than either push or pull motivators used in isolation, and should be considered in the design of training programs, especially for use in animals with inhibited temperaments who are less likely to have high success with appetitive rewards alone [79].
The researchers did not explore the role of social learning in this analysis. Animals have demonstrated the ability to learn at a faster rate after observing conspecifics performing a task, and animals in this research were housed among animals with varying experience with cooperative tasks [81]. Others have shown the role observational learning has in positively shaping animal perceptions of handlers/trainers [82]. The researchers generally find that animals who observe conspecifics having positive interactions with trainers have reduced overall anxiety behaviors related to close human contact. As such, future studies could investigate the effects of the incorporation of social learning on similarly designed training paradigms. As macaques are highly social animals with hierarchical societies, social rank should also be considered as a variable that may have a potential impact on training efficiency during the learning of complex tasks; rank was not analyzed in this research. Such differences have previously been described in rhesus macaques during simple task training [83][84][85].

4. Implications for Welfare and Scientific Validity

Despite individual differences in time to complete training, it is important to note that all animals in the research, regardless of temperament, age, sex, or other demographic characteristics, were able to successfully complete the entire training paradigm and acquire the coping skills necessary for appropriately dealing with exposure to potentially adverse medical situations. In biomedical research, ideal sample choice not only includes selecting the best species for a specific question of interest, but also requires the use of a set of subjects that are as representative of the target population as possible. This has most notably led to a recent push for sex-balancing in scientific studies, but also supports the inclusion of other demographic characteristics, such as temperament, to improve generalizability. Temperament-related selection bias can lead to favoring exploratory animals when candidates are chosen based on preconceived perceptions of their trainability, willingness to cooperate, lack of aggression, and other indicators of affective state [86]. Considering temperament is an interaction between individual biological factors and contextual factors, excluding more inhibited animals in favor of those that are more exploratory has the potential to bias results [7][8][9][10][11]. Despite preconceived notions, the present findings show that inhibited animals can be equally successful at learning a complex training task, and should not be excluded from studies based on perceived study suitability. Using behavioral management as a great equalizer, behaviorally inhibited animals can develop equivalent coping skills to protect their welfare and limit stress bias, so that study populations are more generalizable, improving validity and translatability [36].
Welfare is largely affected by the ways that an animal perceives both its environment and its ability to exert control over it, both of which are closely intertwined with temperament, coping skills, and training. This research shows that well-designed cooperative training has the ability to enable animals of any temperament to develop the coping abilities required to adequately deal with routinely experienced medically necessary aversive situations and reduce consequent stress, demonstrating cooperative training’s critical role in fostering overall welfare in captive animals [68]. Further, training often serves as a form of enrichment, giving animals the chance to perform novel physical and cognitive activities, in addition to providing the opportunity to bond with familiar trainers. Captive animals benefit from the opportunity to learn and perform novel behaviors, and training provides this opportunity [21][87].
An important benefit of successful training is the opportunity for animals to express choice and control over their own care, a key component of welfare. Without proper training, animals often develop a learned helplessness to deal with potentially aversive experiences. Learned helplessness, associated with the inability to escape a stressful situation, can induce uncontrollable, unmediated stress and anxiety [88]. Beyond its ethical implications, the welfare benefits and potential reduction in stress introduced by training can help improve the validity of scientific results and the translational value of the research model. Excess stress has been shown to affect a range of research-related physiologic outcome measures such as heart rate, blood pressure, cortisol, and functional immune state in humans [89][90][91][92], and its reduction through training may lead to a more representative model with less stress-related confounding of results. The researchers have demonstrated previously that the ability to make choices to cooperate with a task, learned during training, fosters a sense of control that is protective psychologically and physically in NHPs [68].

5. Translational Relevance

Beyond its significance for animals in captivity, this research has implications for the management of clinical patients who experience potentially fear-inducing medical procedures for the treatment of a variety of acute and chronic medical conditions. Coping skills training in patients can effectively reduce anxiety and increase compliance with treatment to improve outcomes [93][94][95], but there are gaps in understanding of conditions necessary to support practical treatment options. Primates have become increasingly prominent in understanding biological mechanisms underlying neuropsychiatric disorders, e.g., autism spectrum disorder, emphasizing their relevance in biobehavioral research towards successful interventions [96][97][98]. Behavioral management techniques that foster coping in animals undergoing intensive medical management have strong potential to similarly benefit clinical patients. For example, certain adjustments in management technique for behaviorally inhibited patients, such as reducing the ability to perform avoidance-type behaviors and increasing the opportunity to experience reward while in a controlled setting, could more successfully address the needs of these patients in order to improve coping, foster higher levels of cooperation with medical procedures, and reduce overall stress.

References

  1. Folkman, S.; Moskowitz, J.T. Coping: Pitfalls and promise. Annu. Rev. Psychol. 2004, 55, 745–774.
  2. Leandro, P.G.; Castillo, M.D. Coping with stress and its relationship with personality dimensions, anxiety, and depression. Procedia-Soc. Behav. Sci. 2010, 5, 1562–1573.
  3. Lambert, K.G.; Hyer, M.M.; Rzucidlo, A.A.; Bergeron, T.; Landis, T.; Bardi, M. Contingency-based emotional resilience: Effort-based reward training and flexible coping lead to adaptive responses to uncertainty in male rats. Front. Behav. Neurosci. 2014, 8, 124.
  4. Guidi, J.; Lucente, M.; Sonino, N.; Fava, G.A. Allostatic load and its impact on health: A systematic review. Psychother. Psychosom. 2021, 90, 11–27.
  5. DiMatteo, M.R.; Lepper, H.S.; Croghan, T.W. Depression is a risk factor for noncompliance with medical treatment: Meta-analysis of the effects of anxiety and depression on patient adherence. Arch. Intern. Med. 2000, 160, 2101–2107.
  6. Demyttenaere, K. Risk factors and predictors of compliance in depression. Eur. Neuropsychopharmacol. 2003, 13, 69–75.
  7. Koolhaas, J.M.; Korte, S.M.; De Boer, S.F.; Van Der Vegt, B.J.; Van Reenen, C.G.; Hopster, H.; De Jong, I.C.; Ruis, M.A.W.; Blokhuis, H.J. Coping styles in animals: Current status in behavior and stress-physiology. Neurosci. Biobehav. Rev. 1999, 23, 925–935.
  8. Graves, P.L.; Mead, L.A.; Wang, N.Y.; Liang, K.Y.; Klag, M.J. Temperament as a potential predictor of mortality: Evidence from a 41-year prospective study. J. Behav. Med. 1994, 17, 111–126.
  9. Janowski, K.; Steuden, S. The Temperament Risk Factor, Disease Severity, and Quality of Life in Patients with Psoriasis. Ann. Dermatol. 2020, 32, 452–459.
  10. Sherwood, A.; Blumenthal, J.A.; Koch, G.G.; Hoffman, B.M.; Watkins, L.L.; Smith, P.J.; O’Connor, C.M.; Adams, K.F., Jr.; Rogers, J.G.; Sueta, C.; et al. Effects of Coping Skills Training on Quality of Life, Disease Biomarkers, and Clinical Outcomes in Patients with Heart Failure: A Randomized Clinical Trial. Circ. Heart Fail. 2017, 10, e003410.
  11. Wald, R.L.; Dowling, G.C.; Temoshok, L.R. Coping styles predict immune system parameters and clinical outcomes in patients with HIV. Retrovirology 2006, 3, P65.
  12. Folkman, S. Personal control and stress and coping processes: A theoretical analysis. J. Pers. Soc. Psychol. 1984, 46, 839–852.
  13. D’Onofrio, G.; Simeoni, M.; Rizza, P.; Caroleo, M.; Capria, M.; Mazzitello, G.; Sacco, T.; Mazzuca, E.; Panzino, M.T.; Cerantonio, A.; et al. Quality of life, clinical outcome, personality and coping in chronic hemodialysis patients. Ren. Fail. 2017, 39, 45–53.
  14. Broom, D.M.; Kirkden, R.D. Welfare, stress, behaviour and pathophysiology. Vet. Pathophysiol. 2004, Vol. 1, 337–369.
  15. Veissier, I.; Boissy, A. Stress and welfare: Two complementary concepts that are intrinsically related to the animal’s point of view. Physiol. Behav. 2007, 92, 429–433.
  16. Poole, T. Happy animals make good science. Lab. Anim. 1997, 31, 116–124.
  17. Prescott, M.J.; Lidster, K. Improving quality of science through better animal welfare: The NC3Rs strategy. Lab. Anim. 2017, 46, 152–156.
  18. Koolhaas, J.; Van Reenen, C. Animal behavior and well-being symposium: Interaction between coping style/personality, stress, and welfare: Relevance for domestic farm animals. J. Anim. Sci. 2016, 94, 2284–2296.
  19. Bloomsmith, M.A.; Perlman, J.E.; Hutchinson, E.; Sharpless, M. Behavioral management programs to promote laboratory animal welfare. In Management of Animal Care and Use Programs in Research, Education, and Testing; CRC Press: Boca Raton, FL, USA, 2017; pp. 63–82.
  20. Coleman, K.; Tully, L.A.; McMillan, J.L. Temperament correlates with training success in adult rhesus macaques. Am. J. Primatol. Off. J. Am. Soc. Primatol. 2005, 65, 63–71.
  21. Laule, G.E.; Bloomsmith, M.A.; Schapiro, S.J. The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. J. Appl. Anim. Welf. Sci. 2003, 6, 163–173.
  22. Graham, M.L.; Prescott, M.J. The multifactorial role of the 3Rs in shifting the harm-benefit analysis in animal models of disease. Eur. J. Pharmacol. 2015, 759, 19–29.
  23. Graham, M.L.; Schuurman, H.-J. Validity of animal models of type 1 diabetes, and strategies to enhance their utility in translational research. Eur. J. Pharmacol. 2015, 759, 221–230.
  24. Graham, M.L.; Schuurman, H.-J. Pancreatic islet xenotransplantation. Drug Discov. Today Dis. Models 2017, 23, 43–50.
  25. Ruhe, K.M.; Badarau, D.O.; Brazzola, P.; Hengartner, H.; Elger, B.S.; Wangmo, T. Participation in pediatric oncology: Views of child and adolescent patients. Psychooncology 2016, 25, 1036–1042.
  26. Olszewski, A.E.; Goldkind, S.F. The Default Position: Optimizing Pediatric Participation in Medical Decision Making. Am. J. Bioeth. 2018, 18, 4–9.
  27. Fernström, A.L.; Fredlund, H.; Spångberg, M.; Westlund, K. Positive reinforcement training in rhesus macaques—Training progress as a result of training frequency. Am. J. Primatol. Off. J. Am. Soc. Primatol. 2009, 71, 373–379.
  28. Schapiro, S.J.; Perlman, J.E.; Thiele, E.; Lambeth, S. Training nonhuman primates to perform behaviors useful in biomedical research. Lab. Anim. 2005, 34, 37–42.
  29. Coleman, K. Individual differences in temperament and behavioral management practices for nonhuman primates. Appl. Anim. Behav. Sci. 2012, 137, 106–113.
  30. Balconi, M.; Falbo, L.; Conte, V.A. BIS and BAS correlates with psychophysiological and cortical response systems during aversive and appetitive emotional stimuli processing. Motiv. Emot. 2012, 36, 218–231.
  31. Kagan, J.; Reznick, J.S.; Snidman, N. Biological bases of childhood shyness. Science 1988, 240, 167–171.
  32. Coleman, K.; Pierre, P.J. Assessing anxiety in nonhuman primates. ILAR J. 2014, 55, 333–346.
  33. Graham, M.L. Positive Reinforcement Training and Research; CRC Press: Boca Raton, FL, USA; Taylor & Francis Group: Boca Raton, FL, USA, 2017; Volume 2017.
  34. Prescott, M.J.; Buchanan-Smith, H.M. Training Nonhuman Primates Using Positive Reinforcement Techniques: A Special Issue of the Journal of Applied Animal Welfare Science; Psychology Press: London, UK, 2016.
  35. Roter, D.L. Patient participation in the patient-provider interaction: The effects of patient question asking on the quality of interaction, satisfaction and compliance. Health Educ. Monogr. 1977, 5, 281–315.
  36. Rudolph, K.D.; Dennig, M.D.; Weisz, J.R. Determinants and consequences of children’s coping in the medical setting: Conceptualization, review, and critique. Psychol. Bull. 1995, 118, 328.
  37. Miller, K.S.; Vannatta, K.; Compas, B.E.; Vasey, M.; McGoron, K.D.; Salley, C.G.; Gerhardt, C.A. The role of coping and temperament in the adjustment of children with cancer. J. Pediatr. Psychol. 2009, 34, 1135–1143.
  38. Rothbart, M.K. Temperament, development, and personality. Curr. Dir. Psychol. Sci. 2007, 16, 207–212.
  39. Strelau, J. Temperament risk factor: The contribution of temperament to the consequences of the state of stress. In Extreme Stress and Communities: Impact and Intervention; Springer: Berlin/Heidelberg, Germany, 1995; pp. 63–81.
  40. De Pauw, S.S.; Mervielde, I. Temperament, personality and developmental psychopathology: A review based on the conceptual dimensions underlying childhood traits. Child Psychiatry Hum. Dev. 2010, 41, 313–329.
  41. Williams, P.G.; Suchy, Y.; Rau, H.K. Individual differences in executive functioning: Implications for stress regulation. Ann. Behav. Med. 2009, 37, 126–140.
  42. Keltikangas-Järvinen, L.; Kettunen, J.; Ravaja, N.; Näätänen, P. Inhibited and disinhibited temperament and autonomic stress reactivity. Int. J. Psychophysiol. 1999, 33, 185–196.
  43. Bolhuis, J.E.; Schouten, W.G.; de Leeuw, J.A.; Schrama, J.W.; Wiegant, V.M. Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav. Brain Res. 2004, 152, 351–360.
  44. Rueda, M.R.; Rothbart, M.K. The influence of temperament on the development of coping: The role of maturation and experience. New Dir. Child Adolesc. Dev. 2009, 2009, 19–31.
  45. Turner, C.A.; Flagel, S.B.; Blandino, P.; Watson, S.J.; Akil, H. Utilizing a unique animal model to better understand human temperament. Curr. Opin. Behav. Sci. 2017, 14, 108–114.
  46. Sheynin, J.; Beck, K.D.; Pang, K.C.H.; Servatius, R.J.; Shikari, S.; Ostovich, J.; Myers, C.E. Behaviourally inhibited temperament and female sex, two vulnerability factors for anxiety disorders, facilitate conditioned avoidance (also) in humans. Behav. Process. 2014, 103, 228–235.
  47. Cavigelli, S.A. Behavioral inhibition in rodents: A model to study causes and health consequences of temperament. In Behavioral Inhibition; Springer: Berlin/Heidelberg, Germany, 2018; pp. 35–58.
  48. Hazari, A.; Salberg, S.; Griep, Y.; Yamakawa, G.R.; Mychasiuk, R. Examining changes in rodent temperament following repetitive mild traumatic brain injury in adolescence. Behav. Neurosci. 2020, 134, 384.
  49. Phillips, K.A.; Bales, K.L.; Capitanio, J.P.; Conley, A.; Czoty, P.W.; ‘t Hart, B.A.; Hopkins, W.D.; Hu, S.L.; Miller, L.A.; Nader, M.A. Why primate models matter. Am. J. Primatol. 2014, 76, 801–827.
  50. Zhao, H.; Jiang, Y.H.; Zhang, Y.Q. Modeling autism in non-human primates: Opportunities and challenges. Autism Res. 2018, 11, 686–694.
  51. Camus, S.; Ko, W.K.D.; Pioli, E.; Bezard, E. Why bother using non-human primate models of cognitive disorders in translational research? Neurobiol. Learn. Mem. 2015, 124, 123–129.
  52. Miller, C.; Bard, K.A.; Juno, C.J.; Nadler, R.D. Behavioral responsiveness of young chimpanzees (Pan troglodytes) to a novel environment. Folia Primatol. 1986, 47, 128–142.
  53. Rouff, J.H.; Sussman, R.W.; Strube, M.J. Personality traits in captive lion-tailed macaques (Macaca silenus). Am. J. Primatol. Off. J. Am. Soc. Primatol. 2005, 67, 177–198.
  54. Kagan, J. Temperament and the reactions to unfamiliarity. Child Dev. 1997, 68, 139–143.
  55. Wilson, D.S.; Clark, A.B.; Coleman, K.; Dearstyne, T. Shyness and boldness in humans and other animals. Trends Ecol. Evol. 1994, 9, 442–446.
  56. Kagan, J.; Snidman, N. Early childhood predictors of adult anxiety disorders. Biol. Psychiatry 1999, 46, 1536–1541.
  57. Harper, F.W.; Goodlett, B.D.; Trentacosta, C.J.; Albrecht, T.L.; Taub, J.W.; Phipps, S.; Penner, L.A. Temperament, personality, and quality of life in pediatric cancer patients. J. Pediatr. Psychol. 2014, 39, 459–468.
  58. Archard, G.A.; Braithwaite, V. The importance of wild populations in studies of animal temperament. J. Zool. 2010, 281, 149–160.
  59. DeMaso, D.R.; Snell, C. Promoting coping in children facing pediatric surgery. Semin. Pediatr. Surg. 2013, 22, 134–138.
  60. De Boer, S.F.; Buwalda, B.; Koolhaas, J.M. Untangling the neurobiology of coping styles in rodents: Towards neural mechanisms underlying individual differences in disease susceptibility. Neurosci. Biobehav. Rev. 2017, 74, 401–422.
  61. Zarrabi, F. Investigating the relationship between learning style and metacognitive listening awareness. Int. J. Listening 2020, 34, 21–33.
  62. Davis, S.E. Effects of Motivation, Preferred Learning Styles, and Perceptions of Classroom Climate on Achievement in Ninth and Tenth Grade Math Students. Ph.D. Thesis, University of Florida, Gainesville, FL, USA, 2007.
  63. Webb, L.E.; van Reenen, C.G.; Jensen, M.B.; Schmitt, O.; Bokkers, E.A. Does temperament affect learning in calves? Appl. Anim. Behav. Sci. 2015, 165, 33–39.
  64. Choi, N.; Cho, H.-J. Temperament and home environment characteristics as predictors of young children’s learning motivation. Early Child. Educ. J. 2020, 48, 607–620.
  65. Zimmer-Gembeck, M.J.; Skinner, E.A. The development of coping: Implications for psychopathology and resilience. Dev. Psychopathol. 2016, 1–61.
  66. Blount, R.L.; Simons, L.E.; Devine, K.A.; Jaaniste, T.; Cohen, L.L.; Chambers, C.T.; Hayutin, L.G. Evidence-based assessment of coping and stress in pediatric psychology. J. Pediatr. Psychol. 2008, 33, 1021–1045.
  67. Lyons, D.M.; Parker, K.J.; Schatzberg, A.F. Animal models of early life stress: Implications for understanding resilience. Dev. Psychobiol. 2010, 52, 402–410.
  68. Graham, M.L.; Rieke, E.F.; Mutch, L.A.; Zolondek, E.K.; Faig, A.W.; Dufour, T.A.; Munson, J.W.; Kittredge, J.A.; Schuurman, H.J. Successful implementation of cooperative handling eliminates the need for restraint in a complex non-human primate disease model. J. Med. Primatol. 2012, 41, 89–106.
  69. Manimala, M.R.; Blount, R.L.; Cohen, L.L. The Effects of Parental Reassurance versus Distraction on Child Distress and Coping During Immunizations. Children’s Health Care 2000, 29, 161–177.
  70. Ayers, S.; Baum, A.; McManus, C.; Newman, S.; Wallston, K.; Weinman, J.; West, R. Cambridge Handbook of Psychology, Health and Medicine; Cambridge University Press: Cambridge, UK, 2007.
  71. Connor-Smith, J.K.; Flachsbart, C. Relations between personality and coping: A meta-analysis. J. Pers. Soc. Psychol. 2007, 93, 1080–1107.
  72. Compas, B.E.; Connor-Smith, J.; Jaser, S.S. Temperament, stress reactivity, and coping:implications for depression in childhood and adolescence. J. Clin. Child Adolesc. Psychol. 2004, 33, 21–31.
  73. Freeman, H.D.; Brosnan, S.F.; Hopper, L.M.; Lambeth, S.P.; Schapiro, S.J.; Gosling, S.D. Developing a comprehensive and comparative questionnaire for measuring personality in chimpanzees using a simultaneous top-down/bottom-up design. Am. J. Primatol. 2013, 75, 1042–1053.
  74. Bert, A.; Abbott, D.H.; Nakamura, K.; Fuchs, E. The marmoset monkey: A multi-purpose preclinical and translational model of human biology and disease. Drug Discov. Today 2012, 17, 1160–1165.
  75. Warren, J.M. Possibly unique characteristics of learning by primates. J. Hum. Evol. 1974, 3, 445–454.
  76. Rumbaugh, D.M. Evidence of qualitative differences in learning processes among primates. J. Comp. Physiol. Psychol. 1971, 76, 250.
  77. Box, H. Studies of temperament in simian primates with implications for socially mediated learning. Int. J. Comp. Psychol. 1999, 12, 203–218.
  78. Perone, M. Negative effects of positive reinforcement. Behav. Anal. 2003, 26, 1–14.
  79. Westlund, K. Training laboratory primates—Benefits and techniques. Primate Biol. 2015, 2, 119–132.
  80. Bethell, E.; Holmes, A.; MacLarnon, A.; Semple, S. Cognitive bias in a non-human primate: Husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques. Anim. Welf. 2012, 21, 185–195.
  81. Hopper, L.M. Leveraging Social Learning to Enhance Captive Animal Care and Welfare. J. Zool. Bot. Gard. 2021, 2, 3.
  82. Luna, D.; González, C.; Byrd, C.J.; Palomo, R.; Huenul, E.; Figueroa, J. Do Domestic Pigs Acquire a Positive Perception of Humans through Observational Social Learning? Animals 2021, 11, 127.
  83. Kemp, C.; Thatcher, H.; Farningham, D.; Witham, C.; MacLarnon, A.; Holmes, A.; Semple, S.; Bethell, E.J. A protocol for training group-housed rhesus macaques (Macaca mulatta) to cooperate with husbandry and research procedures using positive reinforcement. Appl. Anim. Behav. Sci. 2017, 197, 90–100.
  84. Wooddell, L.J.; Kaburu, S.S.; Dettmer, A.M. Dominance rank predicts social network position across developmental stages in rhesus monkeys. Am. J. Primatol. 2020, 82, e23024.
  85. Drea, C.M.; Wallen, K. Low-status monkeys “play dumb” when learning in mixed social groups. Proc. Natl. Acad. Sci. USA 1999, 96, 12965–12969.
  86. McKinley, J.; Buchanan-Smith, H.M.; Bassett, L.; Morris, K. Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: Ease of training and time investment. J. Appl. Anim. Welf. Sci. 2003, 6, 209–220.
  87. Coleman, K.; Maier, A. The use of positive reinforcement training to reduce stereotypic behavior in rhesus macaques. Appl. Anim. Behav. Sci. 2010, 124, 142–148.
  88. Vollmayr, B.; Gass, P. Learned helplessness: Unique features and translational value of a cognitive depression model. Cell Tissue Res. 2013, 354, 171–178.
  89. Gasperin, D.; Netuveli, G.; Dias-da-Costa, J.S.; Pattussi, M.P. Effect of psychological stress on blood pressure increase: A meta-analysis of cohort studies. Cad. Saude Publica 2009, 25, 715–726.
  90. Michaud, K.; Matheson, K.; Kelly, O.; Anisman, H. Impact of stressors in a natural context on release of cortisol in healthy adult humans: A meta-analysis. Stress 2008, 11, 177–197.
  91. Schubert, C.; Lambertz, M.; Nelesen, R.A.; Bardwell, W.; Choi, J.B.; Dimsdale, J.E. Effects of stress on heart rate complexity—A comparison between short-term and chronic stress. Biol. Psychol. 2009, 80, 325–332.
  92. Segerstrom, S.C.; Miller, G.E. Psychological stress and the human immune system: A meta-analytic study of 30 years of inquiry. Psychol. Bull. 2004, 130, 601–630.
  93. Pierce, J.S.; Kozikowski, C.; Lee, J.M.; Wysocki, T. Type 1 diabetes in very young children: A model of parent and child influences on management and outcomes. Pediatr. Diabetes 2017, 18, 17–25.
  94. Powers, S.W.; Bloont, R.L.; Bachanas, P.J.; Cotter, M.W.; Swan, S.C. Helping preschool leukemia patients and their parents cope during injections. J. Pediatr. Psychol. 1993, 18, 681–695.
  95. Grey, M.; Whittemore, R.; Jaser, S.; Ambrosino, J.; Lindemann, E.; Liberti, L.; Northrup, V.; Dziura, J. Effects of coping skills training in school-age children with type 1 diabetes. Res. Nurs. Health 2009, 32, 405–418.
  96. Watson, K.K.; Platt, M.L. Of mice and monkeys: Using non-human primate models to bridge mouse-and human-based investigations of autism spectrum disorders. J. Neurodev. Disord. 2012, 4, 21.
  97. Bauman, M.D.; Schumann, C. Advances in nonhuman primate models of autism: Integrating neuroscience and behavior. Exp. Neurol. 2018, 299, 252–265.
  98. Feczko, E.J.; Bliss-Moreau, E.; Walum, H.; Pruett, J.R., Jr.; Parr, L.A. The macaque social responsiveness scale (mSRS): A rapid screening tool for assessing variability in the social responsiveness of rhesus monkeys (Macaca mulatta). PLoS ONE 2016, 11, e0145956.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Video Production Service
Feedback