Evidence of Fear and Anxiety States in Primates
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This article discusses the evidence of fear and anxiety states in primates and their impact on animal welfare. It explores the physiological indicators and the role of non-human primates in studying anxiety and fear. The article also delves into the neurobiological mechanisms and the effects of medication on managing fear and anxiety.
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Running head: ANIMAL BIOLOGY
Discuss the Evidence of Fear and Anxiety States in Primates
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Discuss the Evidence of Fear and Anxiety States in Primates
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Author Note
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1
ANIMAL BIOLOGY
Introduction
Suffering is defined as a state of mind. The level of suffering is difficult to measure
and analyse among the human beings and is also considerably difficult to study among the
animals. The levels of sufferings are associated with the environment in which an individual
live and the physical and mental states of the individual reside. Proper understanding of the
physiology of suffering in animals is important in assessing overall animal welfare. Moreover
it will also help to know the origin of stress and fear in primates (Gregory 2008). The
following review aims of critically analyse the evidences gathered in relation to the state of
anxiety and fear to the primates. Both stress and anxiety falls under the domain of the
negative emotion leading to emotional numbness and generation of natural distress. The
generation of negative emotions and natural distress lead to a change in the behaviour and the
overall psychology causing a significant change in coping skills. Investigation fear and
anxiety among the non-human primates is important as the structure of the brain of primates
is as complex as that to human brains. They also execute similar behavioural and
physiological responses in relation to anxiety and stress (Gregory 2008). Study of anxiety and
stress in non-human primates will open a new gate-way towards understanding the complex
relationship between brain and emotions in human. Moreover, it will also help to understand
the psychological underpinning of primates.
Background of the study
Physiological indicators help in the identification of the individual’s emotional state.
However, interpretation of these behaviours is difficult. For example arousal can be identified
but can have both positive and negative effect on the mental state (Boissy et al. 2007). Barros
et al. (2008) are of the opinion that the behaviour change cause increase in heart rate, increase
in the secretion of endocrine responses along with change in body posture, size of pupil and
ANIMAL BIOLOGY
Introduction
Suffering is defined as a state of mind. The level of suffering is difficult to measure
and analyse among the human beings and is also considerably difficult to study among the
animals. The levels of sufferings are associated with the environment in which an individual
live and the physical and mental states of the individual reside. Proper understanding of the
physiology of suffering in animals is important in assessing overall animal welfare. Moreover
it will also help to know the origin of stress and fear in primates (Gregory 2008). The
following review aims of critically analyse the evidences gathered in relation to the state of
anxiety and fear to the primates. Both stress and anxiety falls under the domain of the
negative emotion leading to emotional numbness and generation of natural distress. The
generation of negative emotions and natural distress lead to a change in the behaviour and the
overall psychology causing a significant change in coping skills. Investigation fear and
anxiety among the non-human primates is important as the structure of the brain of primates
is as complex as that to human brains. They also execute similar behavioural and
physiological responses in relation to anxiety and stress (Gregory 2008). Study of anxiety and
stress in non-human primates will open a new gate-way towards understanding the complex
relationship between brain and emotions in human. Moreover, it will also help to understand
the psychological underpinning of primates.
Background of the study
Physiological indicators help in the identification of the individual’s emotional state.
However, interpretation of these behaviours is difficult. For example arousal can be identified
but can have both positive and negative effect on the mental state (Boissy et al. 2007). Barros
et al. (2008) are of the opinion that the behaviour change cause increase in heart rate, increase
in the secretion of endocrine responses along with change in body posture, size of pupil and
2
ANIMAL BIOLOGY
all these changes might led to either positive or negative outcome on the mental health. In
non-human primates mental health and well-being is guided by 5 different freedoms.
Freedom from the pain, injury and associated disease, freedom from thirst and hunger,
freedom from fear, freedom from discomfort and freedom to express normal behaviour. Fear
and distress or anxiety arise are regarded as negative emotions which hampers the mental
psychology negatively. Stress and pain arise from misery due to exposure to extreme climate,
isolation and physiological problems. Anxiety generates from activity within the limbic
circuits when the ambiguous environmental stimuli is translated as threatening response. Fear
also generates from similar threatening stimuli as it is closely associated with fear. Evidence
highlights that that neural circuitry of fear is associated with anxiety disorder. This causes the
shift of the anxiety focus on the anticipation of a known object or certain unidentifiable
eminent danger (Barros et al 2008). Boissy et al. (2007) are of the opinion the generation of
fear and anxiety among the non-human primates are guided by the Appraisal Theory of
Emotions. This theory is based on the idea that emotions are generated by cognitive
evaluation of the situation. It is process under which all the components like
neurophysiological responses, motor responses, subjective feelings and motivation and
affected causing change in the subjective emotions from time to time (Boissy et al. 2007).
ANIMAL BIOLOGY
all these changes might led to either positive or negative outcome on the mental health. In
non-human primates mental health and well-being is guided by 5 different freedoms.
Freedom from the pain, injury and associated disease, freedom from thirst and hunger,
freedom from fear, freedom from discomfort and freedom to express normal behaviour. Fear
and distress or anxiety arise are regarded as negative emotions which hampers the mental
psychology negatively. Stress and pain arise from misery due to exposure to extreme climate,
isolation and physiological problems. Anxiety generates from activity within the limbic
circuits when the ambiguous environmental stimuli is translated as threatening response. Fear
also generates from similar threatening stimuli as it is closely associated with fear. Evidence
highlights that that neural circuitry of fear is associated with anxiety disorder. This causes the
shift of the anxiety focus on the anticipation of a known object or certain unidentifiable
eminent danger (Barros et al 2008). Boissy et al. (2007) are of the opinion the generation of
fear and anxiety among the non-human primates are guided by the Appraisal Theory of
Emotions. This theory is based on the idea that emotions are generated by cognitive
evaluation of the situation. It is process under which all the components like
neurophysiological responses, motor responses, subjective feelings and motivation and
affected causing change in the subjective emotions from time to time (Boissy et al. 2007).
3
ANIMAL BIOLOGY
Figure: Basic Emotions in Animals
(Source: Barrett, Lewis and Haviland-Jones 2016)
Rational for selecting non-human primate
The rationale behind employing non-human primates as the main model for
investigating anxiety and fear underlines their phylogenetic proximity to humans. Primate
also exhibit identical behavioural and physiological responses to anxiety/fear inducing
situations as human individuals. The complexity of the brain of the primate brain and its
significant resemblance to humans increase the importance behind using primates in
investigating neurobiological mechanisms behind the two most prominent emotions of
human, fear and anxiety (Coleman and Pierre 2014).
ANIMAL BIOLOGY
Figure: Basic Emotions in Animals
(Source: Barrett, Lewis and Haviland-Jones 2016)
Rational for selecting non-human primate
The rationale behind employing non-human primates as the main model for
investigating anxiety and fear underlines their phylogenetic proximity to humans. Primate
also exhibit identical behavioural and physiological responses to anxiety/fear inducing
situations as human individuals. The complexity of the brain of the primate brain and its
significant resemblance to humans increase the importance behind using primates in
investigating neurobiological mechanisms behind the two most prominent emotions of
human, fear and anxiety (Coleman and Pierre 2014).
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ANIMAL BIOLOGY
Critiquing literature
Children with anxious temperament (AT) are regarded to stay under a significant risk
of developing anxiety and depression (Coleman and Pierre 2014). Alisch et al. (2014)
selected young rhesus monkeys, as it is deal for studying the origin of human AT due to its
close resemblance with the humans in the domain of the neural, genetic and phenotypic
underpinnings of the complex emotional and social functioning. Their study is based on the
previous findings which highlighted that the heritability and the functional imaging, along
with the study of the gene expression of AT among the young monkeys is related to central
nucleus of the amygdala (Ce). Ce is projected as the main environmentally sensitive substrate
of this at the risk phenotype. This is because, epigenetic marks (DNA methylation) can be
modified under the effect of the environmental stimuli (Coleman and Pierre 2014). These
data led to a generation of hypothesis of the role of DNA methylation in the generation of the
AT. In order to test this hypothesis, Alisch et al. (2014) used decreased representation
bisulfite sequencing in order to examine the cross-sectional methylation levels in the domain
of Ce among 23 age-matched monkeys under genome wide screening (age group of 1.3 +/-
0.2 years) who are ohenotyped for AT. As AT reflects a continuous variable, the authors used
an analytical approach, which is consistent with this biology for identification of the genes in
the Ce with proper methylation pattern that predicts AT. The expression data from the Ce of
these selected groups of monkeys were then employed to find the differentially methylated
candidates linked to altered level of gene regulation. Two genes are identified which are
significantly relevant to the AT phenotype and these were BCL11A and JAG1. These
transcripts have a well-defined role in the neuro-developmental processes. This also includes
neurite arborisation and proper regulation of the neurogenesis. These findings together
represent an important step towards proper understanding of the effects of the early
environment over the neuro-molecular mechanism that underpins the risk towards
ANIMAL BIOLOGY
Critiquing literature
Children with anxious temperament (AT) are regarded to stay under a significant risk
of developing anxiety and depression (Coleman and Pierre 2014). Alisch et al. (2014)
selected young rhesus monkeys, as it is deal for studying the origin of human AT due to its
close resemblance with the humans in the domain of the neural, genetic and phenotypic
underpinnings of the complex emotional and social functioning. Their study is based on the
previous findings which highlighted that the heritability and the functional imaging, along
with the study of the gene expression of AT among the young monkeys is related to central
nucleus of the amygdala (Ce). Ce is projected as the main environmentally sensitive substrate
of this at the risk phenotype. This is because, epigenetic marks (DNA methylation) can be
modified under the effect of the environmental stimuli (Coleman and Pierre 2014). These
data led to a generation of hypothesis of the role of DNA methylation in the generation of the
AT. In order to test this hypothesis, Alisch et al. (2014) used decreased representation
bisulfite sequencing in order to examine the cross-sectional methylation levels in the domain
of Ce among 23 age-matched monkeys under genome wide screening (age group of 1.3 +/-
0.2 years) who are ohenotyped for AT. As AT reflects a continuous variable, the authors used
an analytical approach, which is consistent with this biology for identification of the genes in
the Ce with proper methylation pattern that predicts AT. The expression data from the Ce of
these selected groups of monkeys were then employed to find the differentially methylated
candidates linked to altered level of gene regulation. Two genes are identified which are
significantly relevant to the AT phenotype and these were BCL11A and JAG1. These
transcripts have a well-defined role in the neuro-developmental processes. This also includes
neurite arborisation and proper regulation of the neurogenesis. These findings together
represent an important step towards proper understanding of the effects of the early
environment over the neuro-molecular mechanism that underpins the risk towards
5
ANIMAL BIOLOGY
development of the anxiety and other depressive disorders (Alisch et al. 2014). One of the
strength of this study is, it helped to understand how the early environment which surrounds
the infants is related towards the development of the depressive disorder while giving a
detailed molecular level mechanism of the DNA methylation in the process of development
of neurones. One of the limitations of this study is, the study mainly highlighted children of
the baby monkeys and thus the result might not have a mass application.
Figure: The Laterality-valence hypothesis
(Source: Barnard et al. 2016)
Social isolation is the main source of stress leading to the generation of anxiety and
fear activation in the hypothalamic-pituitary-adrenal (HPA) axis. The presence of the close
social partner can help to decrease the overall magnitude of the HPA-Axis during a stressor
factor and the phenomenon is known as social buffering (Cacioppo et al. 2015). The oxytocin
(OXT) system is regarded as important candidate for mediating the social buffering because
of its importance in facilitating social bonding and overall expression of prosocial behaviour.
The aim of the study was to determine the contribution of oxytocin towards social buffering
of the HPA-axis activity towards generation of stressor exposure in the marmoset monkeys
ANIMAL BIOLOGY
development of the anxiety and other depressive disorders (Alisch et al. 2014). One of the
strength of this study is, it helped to understand how the early environment which surrounds
the infants is related towards the development of the depressive disorder while giving a
detailed molecular level mechanism of the DNA methylation in the process of development
of neurones. One of the limitations of this study is, the study mainly highlighted children of
the baby monkeys and thus the result might not have a mass application.
Figure: The Laterality-valence hypothesis
(Source: Barnard et al. 2016)
Social isolation is the main source of stress leading to the generation of anxiety and
fear activation in the hypothalamic-pituitary-adrenal (HPA) axis. The presence of the close
social partner can help to decrease the overall magnitude of the HPA-Axis during a stressor
factor and the phenomenon is known as social buffering (Cacioppo et al. 2015). The oxytocin
(OXT) system is regarded as important candidate for mediating the social buffering because
of its importance in facilitating social bonding and overall expression of prosocial behaviour.
The aim of the study was to determine the contribution of oxytocin towards social buffering
of the HPA-axis activity towards generation of stressor exposure in the marmoset monkeys
6
ANIMAL BIOLOGY
(Callithrix jacchus). Thus the study conducted by Cacioppo et al. (2015) aimed in studying
distinct neurological mechanism apart from the central nucleus of the amygdala (Ce) as done
by Alisch et al. (2014). The male and female marmosets experienced an optimal psychogenic
stressor both with and without their long-term mate under the OXT-treatments (Cacioppo et
al. 2015). Cavanaugh et al. (2016) accessed the activity of HPA-axis via measuring the
urinary cortisol across the stressor. The analysis of the results highlighted blocking but not
augmenting under the OXT. OXT is found to alter the patterns of cortisol and proximity
behaviour in relation to stressor. Cavanaugh et al. (2016) also demonstrated that the presence
of a mate during a stressor, attenuates the HPA-axis activity among the female candidates but
have zero effects on the marmosets. However, male but not female, marmosets when treated
with an OXT antagonist have shown higher level of the HPA-axis activity across the stressor
in comparison to the condition when they are treated with saline. This suggested that the
OXT system might decrease the stressor-induced increase in the level of cortisol. Both male
and the female marmosets when treated with an OXT antagonist spent significant less time
under the close proximity to their mate during the first 30 minutes of the stressor in
comparison to when they were treated with saline. This suggests that OXT system might be
an important feature for the expression of the partner-seeking behaviour during the infliction
of the stressor. Thus the authors concluded that the OXT system and the social context helped
in differentially influenced how the HPA-axis properly responded to a stressor factor and
both male and female marmosets and might modulate HPA-axis activity by the promotion of
the expression of the proximity behaviour with a close social partner. Importance of this
study is, it helped in understanding the underlying mechanism of the hormone oxytocin in
modulating the extreme psychological responses of fear, anxiety and behavioural responses
of stress under certain environment of stress (Cavanaugh et al. 2016). One of the limitations
of the study, the study only highlighted the relationship between the male and the female
ANIMAL BIOLOGY
(Callithrix jacchus). Thus the study conducted by Cacioppo et al. (2015) aimed in studying
distinct neurological mechanism apart from the central nucleus of the amygdala (Ce) as done
by Alisch et al. (2014). The male and female marmosets experienced an optimal psychogenic
stressor both with and without their long-term mate under the OXT-treatments (Cacioppo et
al. 2015). Cavanaugh et al. (2016) accessed the activity of HPA-axis via measuring the
urinary cortisol across the stressor. The analysis of the results highlighted blocking but not
augmenting under the OXT. OXT is found to alter the patterns of cortisol and proximity
behaviour in relation to stressor. Cavanaugh et al. (2016) also demonstrated that the presence
of a mate during a stressor, attenuates the HPA-axis activity among the female candidates but
have zero effects on the marmosets. However, male but not female, marmosets when treated
with an OXT antagonist have shown higher level of the HPA-axis activity across the stressor
in comparison to the condition when they are treated with saline. This suggested that the
OXT system might decrease the stressor-induced increase in the level of cortisol. Both male
and the female marmosets when treated with an OXT antagonist spent significant less time
under the close proximity to their mate during the first 30 minutes of the stressor in
comparison to when they were treated with saline. This suggests that OXT system might be
an important feature for the expression of the partner-seeking behaviour during the infliction
of the stressor. Thus the authors concluded that the OXT system and the social context helped
in differentially influenced how the HPA-axis properly responded to a stressor factor and
both male and female marmosets and might modulate HPA-axis activity by the promotion of
the expression of the proximity behaviour with a close social partner. Importance of this
study is, it helped in understanding the underlying mechanism of the hormone oxytocin in
modulating the extreme psychological responses of fear, anxiety and behavioural responses
of stress under certain environment of stress (Cavanaugh et al. 2016). One of the limitations
of the study, the study only highlighted the relationship between the male and the female
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ANIMAL BIOLOGY
attention seeking attitudes towards overcoming the stress and anxiety. The study failed to
analyze the underlying the neuro-biological mechanism towards managing of the stress.
However, reference of the modulation of the level of cortisol and oxytocin in stress and fear
management open the gateway towards the effect of endocrine system in managing emotions.
Raper et al (2015) conducted a study with an aim to study the whether the repeated
exposure to the anaesthetic exposure is effective in causing a long-term behavioural changes
under a highly translationallly relevant rhesus monkey, enabling study of these variables
against the backdrop of the generation of fear and anxiety. Raper et al (2015) used Rhesus
monkeys of both sex and treated them with sevoflurance aesthesia for at least 4 hours
followed by a brief maternal separation during the 6 to 10th day of the post-natal period. The
same scenario was repeated after 14 and 28 days. Monkeys mainly remained with their
mother under the large social groups during all time expect during the over-night observation
following each anaesthetic treatment. When the baby monkeys are of 6 months of age, they
are tested under the human intruder paradigm, a common test used for testing of the
emotional activity in the non-human primates. The analysis of the results highlighted that the
frequency of the anxiety-related behaviours is significantly high among the monkeys when
they are exposed the anaesthesia in comparison to the neonates. Finally Raper et al (2015)
concluded that the increased emotional behaviour in monkeys after the anaesthesia exposure
during the infancy might reflected the long-term adverse effects of anaesthesia (Raper et al
2015). Apart from the effect of the oxytocin in the fear and anxiety among the non-human
primate is also modulated by other medications. Administration of apo-diazepam (DZP) at
2 mg/kg helps in reversing the fear-induced avoidance by inflicting aversive stimulus.
0.5 mg/kg of buspirone also found to induce similar mechanism in non-human primates in
stimulation fear induced avoidance. One of the strength of the study is both models have
ANIMAL BIOLOGY
attention seeking attitudes towards overcoming the stress and anxiety. The study failed to
analyze the underlying the neuro-biological mechanism towards managing of the stress.
However, reference of the modulation of the level of cortisol and oxytocin in stress and fear
management open the gateway towards the effect of endocrine system in managing emotions.
Raper et al (2015) conducted a study with an aim to study the whether the repeated
exposure to the anaesthetic exposure is effective in causing a long-term behavioural changes
under a highly translationallly relevant rhesus monkey, enabling study of these variables
against the backdrop of the generation of fear and anxiety. Raper et al (2015) used Rhesus
monkeys of both sex and treated them with sevoflurance aesthesia for at least 4 hours
followed by a brief maternal separation during the 6 to 10th day of the post-natal period. The
same scenario was repeated after 14 and 28 days. Monkeys mainly remained with their
mother under the large social groups during all time expect during the over-night observation
following each anaesthetic treatment. When the baby monkeys are of 6 months of age, they
are tested under the human intruder paradigm, a common test used for testing of the
emotional activity in the non-human primates. The analysis of the results highlighted that the
frequency of the anxiety-related behaviours is significantly high among the monkeys when
they are exposed the anaesthesia in comparison to the neonates. Finally Raper et al (2015)
concluded that the increased emotional behaviour in monkeys after the anaesthesia exposure
during the infancy might reflected the long-term adverse effects of anaesthesia (Raper et al
2015). Apart from the effect of the oxytocin in the fear and anxiety among the non-human
primate is also modulated by other medications. Administration of apo-diazepam (DZP) at
2 mg/kg helps in reversing the fear-induced avoidance by inflicting aversive stimulus.
0.5 mg/kg of buspirone also found to induce similar mechanism in non-human primates in
stimulation fear induced avoidance. One of the strength of the study is both models have
8
ANIMAL BIOLOGY
yielded consistent, pronounced and most significant results by employing distinct drug
treatments among the non-human primates (Barros and Tomaz 2002).
Conclusion
Thus from the critique of the literature conducted above it can be concluded that the
non-human primates also exhibit negative emotions of fear and anxiety like the human and
these emotions are appraised by complex neuro-biological pathway and can be modulates by
administration of medication. The generation of the negative emotions of fear and anxiety is
modulated by the DNA methylation by epigenetic patterns in the Ce along with the perceived
environment in the early childhood. apart from Ce, HPA axis also promotes the appraisal of
the negative emotions under the stressor factor. Proper administration of the OXT promotes
social buffering and thereby helping to decrease the severity of the negative emotions. The
study of the literature also revealed that the use of anaesthesia might not be suitable to
management of the negative emotions unlike the human as it increase the sense of the
emotional behaviours as experienced by the Rhesus monkeys. Administration of the other
medication like the buspirone and apo-diazepam (DZP) is found to provide positive results.
ANIMAL BIOLOGY
yielded consistent, pronounced and most significant results by employing distinct drug
treatments among the non-human primates (Barros and Tomaz 2002).
Conclusion
Thus from the critique of the literature conducted above it can be concluded that the
non-human primates also exhibit negative emotions of fear and anxiety like the human and
these emotions are appraised by complex neuro-biological pathway and can be modulates by
administration of medication. The generation of the negative emotions of fear and anxiety is
modulated by the DNA methylation by epigenetic patterns in the Ce along with the perceived
environment in the early childhood. apart from Ce, HPA axis also promotes the appraisal of
the negative emotions under the stressor factor. Proper administration of the OXT promotes
social buffering and thereby helping to decrease the severity of the negative emotions. The
study of the literature also revealed that the use of anaesthesia might not be suitable to
management of the negative emotions unlike the human as it increase the sense of the
emotional behaviours as experienced by the Rhesus monkeys. Administration of the other
medication like the buspirone and apo-diazepam (DZP) is found to provide positive results.
9
ANIMAL BIOLOGY
References
Alisch, R.S., Chopra, P., Fox, A.S., Chen, K., White, A.T., Roseboom, P.H., Keles, S. and
Kalin, N.H., 2014. Differentially methylated plasticity genes in the amygdala of young
primates are linked to anxious temperament, an at risk phenotype for anxiety and depressive
disorders. Journal of Neuroscience, 34(47), pp.15548-15556.
Barnard, S., Matthews, L., Messori, S., Podaliri-Vulpiani, M. and Ferri, N., 2016. Laterality
as an indicator of emotional stress in ewes and lambs during a separation test. Animal
cognition, 19(1), pp.207-214.
Barrett, L.F., Lewis, M. and Haviland-Jones, J.M. eds., 2016. Handbook of emotions.
Guilford Publications.
Barros, M. and Tomaz, C., 2002. Non-human primate models for investigating fear and
anxiety. Neuroscience & Biobehavioral Reviews, 26(2), pp.187-201.
Boissy, A., Arnould, C., Chaillou, E., Désiré, L., Duvaux-Ponter, C., Greiveldinger, L.,
Leterrier, C., Richard, S., Roussel, S., Saint-Dizier, H. and Meunier-Salaün, M.C., 2007.
Emotions and cognition: a new approach to animal welfare. Animal Welfare, 16(2), pp.37-43.
Cacioppo, J.T., Cacioppo, S., Capitanio, J.P. and Cole, S.W., 2015. The neuroendocrinology
of social isolation. Annual review of psychology, 66, pp.733-767.
Cavanaugh, J., Carp, S.B., Rock, C.M. and French, J.A., 2016. Oxytocin modulates
behavioral and physiological responses to a stressor in marmoset
monkeys. Psychoneuroendocrinology, 66, pp.22-30.
Coleman, K. and Pierre, P.J., 2014. Assessing anxiety in nonhuman primates. Ilar
Journal, 55(2), pp.333-346.
ANIMAL BIOLOGY
References
Alisch, R.S., Chopra, P., Fox, A.S., Chen, K., White, A.T., Roseboom, P.H., Keles, S. and
Kalin, N.H., 2014. Differentially methylated plasticity genes in the amygdala of young
primates are linked to anxious temperament, an at risk phenotype for anxiety and depressive
disorders. Journal of Neuroscience, 34(47), pp.15548-15556.
Barnard, S., Matthews, L., Messori, S., Podaliri-Vulpiani, M. and Ferri, N., 2016. Laterality
as an indicator of emotional stress in ewes and lambs during a separation test. Animal
cognition, 19(1), pp.207-214.
Barrett, L.F., Lewis, M. and Haviland-Jones, J.M. eds., 2016. Handbook of emotions.
Guilford Publications.
Barros, M. and Tomaz, C., 2002. Non-human primate models for investigating fear and
anxiety. Neuroscience & Biobehavioral Reviews, 26(2), pp.187-201.
Boissy, A., Arnould, C., Chaillou, E., Désiré, L., Duvaux-Ponter, C., Greiveldinger, L.,
Leterrier, C., Richard, S., Roussel, S., Saint-Dizier, H. and Meunier-Salaün, M.C., 2007.
Emotions and cognition: a new approach to animal welfare. Animal Welfare, 16(2), pp.37-43.
Cacioppo, J.T., Cacioppo, S., Capitanio, J.P. and Cole, S.W., 2015. The neuroendocrinology
of social isolation. Annual review of psychology, 66, pp.733-767.
Cavanaugh, J., Carp, S.B., Rock, C.M. and French, J.A., 2016. Oxytocin modulates
behavioral and physiological responses to a stressor in marmoset
monkeys. Psychoneuroendocrinology, 66, pp.22-30.
Coleman, K. and Pierre, P.J., 2014. Assessing anxiety in nonhuman primates. Ilar
Journal, 55(2), pp.333-346.
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ANIMAL BIOLOGY
Gregory, N.G., 2008. Physiology and behaviour of animal suffering. John Wiley & Sons.
Raper, J., Alvarado, M.C., Murphy, K.L. and Baxter, M.G., 2015. Multiple anesthetic
exposure in infant monkeys alters emotional reactivity to an acute stressor. The Journal of the
American Society of Anesthesiologists, 123(5), pp.1084-1092.
ANIMAL BIOLOGY
Gregory, N.G., 2008. Physiology and behaviour of animal suffering. John Wiley & Sons.
Raper, J., Alvarado, M.C., Murphy, K.L. and Baxter, M.G., 2015. Multiple anesthetic
exposure in infant monkeys alters emotional reactivity to an acute stressor. The Journal of the
American Society of Anesthesiologists, 123(5), pp.1084-1092.
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