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Journal of Trauma & Dissociation
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Parallels in Sources of Trauma, Pain,
Distress, and Suffering in Humans and
Nonhuman Animals
Hope Ferdowsian MDMPH
a
& Debra Merskin PhD
b
a
Physician's Committee for Responsible Medicine; Department of
Medicine, George Washington University, Washington, DC, USA
b
School of Journalism & Communication, University of Oregon,
Eugene, Oregon, USA
Available online: 24 Jan 2012
To cite this article: Hope Ferdowsian MDMPH & Debra Merskin PhD (2012): Parallels in Sources
of Trauma, Pain, Distress, and Suffering in Humans and Nonhuman Animals, Journal of Trauma &
Dissociation, 13:4, 448-468
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Journal of Trauma & Dissociation, 13:448468, 2012
Copyright Taylor & Francis Group, LLC
ISSN: 1529-9732 print/1529-9740 online
DOI: 10.1080/15299732.2011.652346
Parallels in Sources of Trauma, Pain,
Distress, and Suffering in Humans
and Nonhuman Animals
HOPE FERDOWSIAN, MD, MPH
Physicians Committee for Responsible Medicine; Department of Medicine, George
Washington University, Washington, DC, USA
DEBRA MERSKIN, PhD
School of Journalism & Communication, University of Oregon, Eugene, Oregon, USA
It is widely accepted that animals often experience pain and
distress as a result of their use in scientic experimentation.
However, unlike human suffering, the wide range of acute, recur-
rent, and chronic stressors and trauma on animals is rarely
evaluated. In order to better understand the cumulative effects
of captivity and laboratory research conditions on animals, we
explore parallels between human experiences of pain and psy-
chological distress and those of animals based on shared brain
structures and physiological mechanisms. We review anatomical,
physiological, and behavioral similarities between humans and
other animals regarding the potential for suffering. In addition,
we examine associations between research conditions and indica-
tors of pain and distress. We include 4 case studies of common
animal research protocols in order to illustrate incidental and
experimental factors that can lead to animal suffering. Finally,
we identify parallels between established traumatic conditions for
humans and existing laboratory conditions for animals.
KEYWORDS distress, ethics, posttraumatic stress, stress
It is widely acknowledged that nonhuman animals (hereafter, animals)
often experience pain and distress in the course of their use in scien-
tic experimentation (Gregory, 2004; Recognition, 2009). However, human
Received 11 August 2011; accepted 20 October 2011.
Address correspondence to Debra Merskin, PhD, School of Journalism & Communi-
cation, University of Oregon, Eugene, OR 97403. E-mail: dmerskin@uoregon.edu
448
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Journal of Trauma & Dissociation, 13:448468, 2012 449
interventions to minimize pain and distress in animals commonly focus on
reducing the numbers of animals used and making changes to specic pro-
tocols rather than evaluating the suffering individual animals experience
over the course of their lifetimes. This differs from the consideration of
human suffering, in which researchers examine the impact of acute, recur-
rent, and chronic trauma on individuals. Because animals are frequently used
in research, there is an ethical imperative to better understand the cumulative
effects of captivity and the rigors of laboratory research on animals.
In 1789, moral philosopher and legal scholar Jeremy Bentham noted
that it is the ability to suffer, not the ability to reason, that should be the
insuperable line (1789/1836, p. 236) that determines the treatment of other
beings, including infants, adults with particular disabilities, and animals.
According to Bentham,
A full-grown horse or dog is beyond comparison a more rational, as well
as a more conversable animal, than an infant of a day or a week or even
a month, old. But suppose the case were otherwise, what would it avail?
The question is not, Can they reason? Nor, Can they talk? But, can they
suffer? (p. 236)
Knowledge of pain, psychological distress, and suffering in humans and
other animals has evolved signicantly since Benthams statement was rst
published. Only in relatively recent history have scientists and physicians
acknowledged that human infants experience pain (Bellieni & Buonocore,
2010; Chamberlain, 1989). Furthermore, some have suggested that babies
and young children may experience more pain than adults because they
have not yet developed a mechanism that may reduce pain severity
(Dombrowski, 1997; Pluhar, 1993). As articulated by the International
Association for the Study of Pain (2007), Pain is always subjective, and
the inability to communicate verbally does not negate the possibility that an
individual is experiencing pain (Merskey & Bogduk, 1994, p. 211). Although
this statement was intended to apply to infants and other humans unable to
articulate their experiences, it can also be applied to nonhuman animals.
Suffering has been characterized in several ways. For example,
DeGrazia (2002) has posited that suffering occurs when the source of pain is
unknown, when the meaning of the pain is dire, or when the pain is appar-
ently without end (p. 35). Suffering has been dened as an unpleasant
subjective experience (Singer, 2006) or a state of severe distress associ-
ated with events that threaten the intactness of the person (Cassell, 2004,
p. 32). Although sometimes used synonymously with physical pain, suffer-
ing can also originate and manifest psychologically. Perhaps more broadly,
suffering has been described by Morton and Hau (2002, p. 459) as a nega-
tive emotional state which derives from adverse physical, physiological, and
psychological circumstances, in accordance with the cognitive capacity of
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450 H. Ferdowsian and D. Merskin
the species and the individual being, and its lifes experience. Dawkins
(2008) has suggested that animal suffering can be measured empirically
through the evaluation of emotional states, as indicated by behavioral and
physiological parameters. Suffering can be dened as a set of negative emo-
tions such as fear and pain and recognized operationally as states caused
by negative reinforcers (Dawkins, 2008). Thus, suffering can manifest as
physical or mental experiences or both.
Here we address the following questions, drawing on Bentham
(1789/1836): In what ways do animals suffer physically and psychologically
as a result of their use in laboratory research, and what are some of the gen-
eral factors that can lead to their suffering? In order to address our central
questions, we review anatomical, physiological, and behavioral similarities
between humans and other animals as they relate to the capacity for pain,
psychological distress, and suffering. We draw upon an evolutionary frame-
work that acknowledges convergence and divergence across species (Brne,
2008; Cantor & Joyce, 2009; Marino, 2002; Stevens & Price, 2000). We also
explore evidence regarding the association between laboratory research con-
ditions, including captivity, and indicators of pain and psychological distress.
We identify parallels between established traumatic conditions for humans
and existing laboratory conditions for animals. Finally, we examine four case
studies of common animal research protocols in order to illustrate research
conditions that can lead to animal suffering.
COMMON PAIN PATHWAYS IN HUMANS AND ANIMALS
Despite the obvious challenge posed by the fact that animals are generally
unable to report their physical and emotional states to humans, studies from
multiple disciplines provide objective evidence of animals abilities to expe-
rience pain. In fact, much of what experts understand about animal pain
stems from studies in which animals were intentionally exposed to painful
or distressful experiences.
Partially as a result of homologous anatomical structures and physio-
logical mechanisms, animals demonstrate coordinated responses to pain and
many emotional states and responses that are similar to those of humans.
As dened by the International Association for the Study of Pain (2007), pain
is an unpleasant sensory and emotional experience associated with actual
or potential tissue damage, or described in terms of such damage (p. 1979).
In its specic application to animals, Zimmermann (1986, p. 16) modied
the denition to include an aversive sensory experience caused by actual or
potential injury that elicits progressive motor and vegetative reactions, results
in learned avoidance behavior, and may modify species-specic behavior,
including social behavior.
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Journal of Trauma & Dissociation, 13:448468, 2012 451
Anatomical and Physiological Similarities
In vertebrates, pain and proprioception are mediated by somatosensory
neurons of the trigeminal and dorsal root ganglia, which terminate in the
skin and other tissues. Somatosensory stimuli trigger electrical impulses that
are interpreted by the central nervous system (Lumpkin & Bautista, 2005).
Invertebrates have also demonstrated coordinated responses to painful stim-
uli. Cephalopods, such as octopuses, demonstrate well-organized nervous
systems that include brain centers concerned with sensory analysis, memory,
learning, and decision making (Hochner, Shomrat, & Fiorito, 2006; Mather,
2008). These areas of the cephalopod brain have been compared with the
cerebral cortex of vertebrates. As Mather (2008) has suggested, the conver-
gence of brain functions of invertebrate brains to those of vertebrates may
be even more relevant than anatomical comparisons.
Rather than taking a scala naturae or hierarchal approach, one can
explain similarities and differences in emotional processes across species
by the ways in which humans and animals have adapted to different eco-
logical niches (Shettleworth, 1998). Analgesics can modify pain responses
in animals as they do in humans. Pain may result in physiological changes
involving the heart, kidneys, immune system, and other organ systems that
are critical to disease progression and recovery (Gregory, 2004). Animals can
experience acute or immediate pain, as well as slow crescendo pain, such as
the pain of inammation, visceral pain, and neuropathic pain. Although the
nociceptive pathways of pain are fairly well described, the molecular mech-
anisms involved in pain perception and the neurological responses to tissue
and neuronal injury are not well understood in humans or other animals.
This complicates the ability to adequately prevent, recognize, and treat pain
in animals. The pain and discomfort associated with disease (also called
sickness behavior) can be at least partially explained by shared cytokine-
mediated responses that can result in lethargy, depression, anorexia, sleep
disturbances, and enhanced sensitivity to pain (Dantzer & Kelley, 2007).
Cytokines have sickness-inducing properties, partly as a result of the acti-
vation of the hypothalamicpituitaryadrenal (HPA) axis. Sickness behavior
occurs in mammals and birds (Dantzer & Kelley, 2007), and it is now under-
stood that communication systems that link the immune and central nervous
systems, although nonspecic, are biologically critical for survival and recov-
ery. However, the sickness response can become maladaptive, resulting in a
variety of chronic inammatory diseases and depression.
Pain may be experienced differently depending on genetic and environ-
mental differences. Genotype may affect susceptibility to heat or other forms
of pain, and sensitivity to pain and pain-related traits may in part be heri-
table (Lariviere & Mogil, 2010). Factors such as sleep deprivation have also
been associated with pain perception, although the direction of causality is
sometimes unclear (Lautenbacher, Kundermann, & Krieg, 2006). In addition
to individual differences, other physical and psychological stressors can
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452 H. Ferdowsian and D. Merskin
contribute signicantly to the perception of pain as well as to an individuals
ability to cope with pain.
Behavioral Similarities
Animals express pain in ways similar to humans, including through
avoidance behaviors, abnormal postures, guarding to protect an affected
area, vocalizations such as whimpering, aggression, and physiological and
endocrine responses, among others (Gregory, 2004). Furthermore, the antic-
ipation of pain can result in mood and behavioral changes that exacerbate
psychological distress (Ploghaus et al., 1999).
Behavioral observations have been important in ascertaining when
and how animals experience pain. However, just as there are variations
in the expression of suffering within human populations, there are also
differences across species and between individual animals. Because of evo-
lutionary pressures, some animals may be more likely than others to use
certain response behaviors. For example, many animals develop mecha-
nisms that suppress signs of acute and chronic pain, particularly during times
of extreme fear (Gregory, 2004; McGowan, Stubbs, & Goff, 2007). Animals
vulnerable to predation may attempt to hide signs of pain in attempts to
enhance survival (Moberg & Mench, 2000) but may experience psychological
sequelae. Animals often exhibit fearful, avoidant, and hypervigilant behav-
iors considered parallel to those expressed by traumatized humans (Cohen,
Matar, Richter-Levin, & Zohar, 2006).
PSYCHOLOGICAL DISTRESS AND PSYCHOPATHOLOGY
The brain demonstrates signicant plasticity. Although form and function
are guided by genetic factors, environment and experiences help shape
brain structure, function, and activity. In anxiety and depressive disorders,
the combination of stressors overwhelms normal physiological responses,
sometimes causing structural and physiological changes. The structures and
neuroendocrine mechanisms associated with these conditions are shared
across a wide range of animals.
Fear, anxiety, and relevant reactions and responses serve as an organ-
isms rst line of defense (Kim & Gorman, 2005; Lang, Davis, & Ohman,
2000). Some of these responses are dependent upon the activation of a
common subcortical circuit (Lang et al., 2000; Panksepp, 2004). As a result,
reactions associated with fear occur much more quickly than do slower,
language-based appraisals (Lang et al., 2000). The absence of certain neu-
rological structures may also be relevant to suffering because animals with
less organized neural circuits may demonstrate less exibility and have more
limited coping mechanisms. Some animals may suffer more than humans
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Journal of Trauma & Dissociation, 13:448468, 2012 453
would in an analogous situation because of their inability to understand
what is happening to them, make sense of their plight, escape from it, or
alter their conditions.
Mammals share a large number of brain regions associated with emo-
tional affect, including the amygdala, hippocampus, hypothalamus, and
prefrontal cortex, among other areas (Broom, 2010; Murray, 2007; Panksepp,
1982, 1998, 2004; Rolls, 2005). As a result, there are homologies in attach-
ment disorders, depression, complex anxiety disorders, and persistent
disorders of social behavior (Brne, 2008). For example, fear responses are
stored as memories and linked to the amygdala and can be expressed in
mammals as anxiety disorders and specic phobias (Brne, Brne-Cohrs,
McGrew, & Preuschoft, 2006; Kim & Gorman, 2005). The hippocampus,
found in all vertebrates, is involved in memory storage and retrieval and may
explain some of the similarities in chronic psychopathology across species.
In humans and other animals, chronic posttraumatic stress has been asso-
ciated with decreased hippocampal volumes (Gregory, 2004) and changes
to other areas of the brain, including the prefrontal cortex (Gregory, 2004;
Otani, 2004), perhaps because of recurrently and chronically elevated lev-
els of cortisol, followed by downregulation of the HPA axis (Cohen et al.,
2006; Gregory, 2004). Abnormalities of the HPA axis have been identied
in animals who have been conned, restrained, or isolated and after sur-
gical procedures (Gregory, 2004). Moreover, studies have indicated that
hypothalamic nerve growth factor levels are responsive to and modied by
psychological stimuli, most likely associated with anxiety and fear (Alleva
& Francia, 2009). Similar anatomical changes have also been noted across
species. For example, captivity of only a few weeks duration can reduce the
volume of the hippocampus of birds by as much as 23% (Tarr, Rabinowitz,
Imtiaz, & DeVoogd, 2009), potentially resulting in memory decits.
Variations of posttraumatic stress disorder have been described in chim-
panzees and other animals (Bradshaw, Capaldo, Lindner, & Grow, 2008;
Brne et al., 2006; Ferdowsian et al., 2011). Mice show persistent fear and
increases in sensitized fear related to hyperarousal, emotional blunting, and
social withdrawal, as seen in posttraumatic stress disorder (Siegmund &
Wotjak, 2006). A study of juvenile rats designed to model childhood trauma
found that exposing the rats to litter soaked in predator (cat) urine increased
the likelihood that they would develop long-term behavioral disruptions
thought to represent posttraumatic stress symptom equivalents. When the
rats were exposed a second time in adulthood, the responses persisted
(Cohen et al., 2006).
Researchers have also described signs of depression in animals, includ-
ing nonhuman primates, dogs, pigs, cats, birds, and rodents, among others.
For example, learned helplessness and other characteristics of depres-
sion, such as anhedonia, have been described in mice and other animals
(Strekalova, Spanagel, Bartsch, Henn, & Gass, 2004). Mice also demonstrate
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454 H. Ferdowsian and D. Merskin
empathic responses when painful stimuli are inicted on individuals they
know (Langford et al., 2006).
THE EFFECTS OF CAPTIVITY AND LABORATORY CONDITIONS
Pain and distress are commonly experienced in the laboratory as a result
of experimental protocols or incidentally (Balcombe, Barnard, & Sandusky,
2004; Carbone, 2004; Newcomer, 2000; Panksepp, 2004). Potential sources
of pain and distress are present from birth (or even the prenatal period) to
death and can include birth conditions, maternal separation, connement,
cage transfers, handling, painful procedures, social isolation, restraint, and
deprivation of simple needs (e.g., adequate sleep, food, water, and shel-
ter). For use in research, animals are regularly transported from a breeding
facility or natural habitat to a laboratory. Animals also experience social
deprivation, the inability to fulll natural behaviors (e.g., hygienic practices,
natural movement), lack of natural habitat, conditions of over- or understim-
ulation, and witnessing of harming and killing of peers. Many of these factors
resemble potentially traumatic conditions and consequences of human cap-
tivity that have been described elsewhere (Brenner, 2010). Here we explore
parallels between traumatic conditions for humans and common laboratory
conditions for animals and explore the similar pathologies resulting from
these conditions. Table 1 also illustrates cross-species parallels regarding the
potential for physical and psychological trauma.
Severed Bonds and Social Deprivation
Animals of many species rely upon early parental support for their devel-
opment. Animals also commonly form bonds with conspecics for adequate
TABLE 1 Common Potential Sources of Trauma in Humans and Other Animals
Physical trauma Psychological trauma
Deprivation of basic needs, including
water, food, sunlight, and sleep
Social deprivation and neglect or social
pressures
Withholding of adequate nutrition Isolation or inability to seek solitude
Inadequate provision of shelter, sanitation,
and hygiene
Sensory deprivation or overstimulation
Restriction of physical activity or exercise Deprivation of the ability to fulll
natural behaviors or loss of autonomy
Invasive procedures, including sharp and
blunt trauma, burns, induced diseases,
unnecessary surgical procedures, and
forms of death
Threats to physical integrity or threats
of death
Withholding of adequate health care Witnessing of painful or distressful
procedures
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Journal of Trauma & Dissociation, 13:448468, 2012 455
social support and development. Among both humans and animals, if a par-
ent is not present early in life, offspring are likely to develop stereotypic
behaviors (Bowlby, 1969, 1973, 1980; Latham & Mason, 2008). Maternally
deprived animals develop a suite of changes in neurotransmitter activity and
anxiety and stress responses, including increases in stereotypic behaviors
(Gregory, 2004; Latham & Mason, 2008; Lutz, Well, & Novak, 2003; Mason,
2008).
Although developmental periods vary widely by species, deprivation-
induced stereotypic behaviors are fairly typical. It is common for laboratory
animals to be separated from their mothers earlier than would be the case
if they were free living (Latham & Mason, 2008). Interruption in maternal
care, or restricted access to mothers who are sometimes less able to care
for their young because they themselves were also maternally deprived, cre-
ates distress in animals that can extend beyond infancy and adolescence.
For example, laboratory mice are typically separated from their mothers
at 20 days (Wrbel & Stauffacher, 1997), whereas free-living rodents are
weaned around 35 days (Latham & Mason, 2004). Bar biting and other abnor-
mal behaviors have been described in mice used in laboratory research as
a response to premature weaning, thwarted attempts to suckle, or unpleas-
ant cage experiences (Callard, Bursten, & Price, 1999; Waiblinger & Konig,
2004; Wrbel & Stauffacher, 1997). Among mouse pups, precocious wean-
ing contributes to anxiety and aggression (Kikusui, Isaka, & Mori, 2005).
Kittens who are removed too early from their mothers often display anxi-
ety and exhibit wool-sucking behaviors (Bowen & Heath, 2005). Premature
separation from mothers also leads to a range of adverse behavioral and
social effects in primate infants (Dettling, Feldon, & Pryce, 2002; Harlow,
Dodsworth, & Harlow, 1965; Novak, Meyer, Lutz, & Tiefenbacher, 2006;
C. M. Rogers & Davenport, 1969). Stereotypic and self-directed behaviors
have been described in peer-reared rhesus macaques and chimpanzees, par-
ticularly those who spent their rst few months in incubators (Bloomsmith,
Baker, Ross, & Pazol, 2002; Champoux, Metz, & Suomi, 1991; Erwin, 1986;
Lutz et al., 2003).
Prolonged Isolation and Sensory Deprivation
Among humans, solitary connement is associated with increased risk for
psychopathology, including symptoms of depression and anxiety (Andersen
et al., 2000; Brenner, 2010). Even in conditions in which they choose to be in
a temporarily isolating environment, such as polar expeditions, individuals
frequently experience depression, anxiety, paranoia, and physical symptoms
such as headaches and impaired cognition (Suedfeld & Steel, 2000).
Animals who are purposefully bred for research or captured from the
wild are routinely conned to cages prior to and during experimental pro-
tocols. Cats, dogs, rodents, nonhuman primates, and other animals are
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456 H. Ferdowsian and D. Merskin
inherently social but are frequently kept under conditions of prolonged iso-
lation and sensory deprivation. As a result, animals can exhibit abnormal
behaviors such as whole-body stereotypies and self-mutilation, which can
be traced to maternal deprivation, connement, sensory deprivation, isola-
tion, and other laboratory experiences (Avgustinovich & Kovalenko, 2005;
Brne et al., 2006; Latham & Mason, 2008; Lutz et al., 2003). Standard lab-
oratory housing also appears to cause changes in nonhuman primates and
rodents brain regions (Kozorovitskiy et al., 2005) important to memory, such
as the hippocampus.
Isolation and lack of social stimulation can contribute to distress, par-
ticularly among animals whose natural behaviors are highly social and
involve seeking and play (Smith & Taylor, 1996). For example, tail biting,
stereotypies, and neurotic behaviors are often exhibited in pigs without
access to stimulation (Rollin & Kesel, 1995). Littermate-deprived kittens have
demonstrated prolonged separation effects and failed to develop social com-
munication skills (Guyot, Bennett, & Cross, 1980; Guyot, Cross, & Bennett,
1980). Dogs who are isolated and deprived of sensory stimulation also
exhibit a variety of behavioral pathologies ranging from crying to domi-
nance aggression (Gregory, 2004; Panksepp, Herman, Conner, Bishop, &
Scott, 1978). Other manifestations in dogs, such as fear, generalized anxi-
ety, obsessive-compulsive disorder, predatory aggression, noise phobia, and
impulse control, often appear in the rst few years of life when neural
systems are maturing (Overall, 1994, 2005; Overall & Dunham, 2002).
Sensory Overstimulation, Sleep Deprivation, and Circadian Cycle
Disruption
Exposure to orescent light and disruption of sleep cycles are typical tools
in the interrogation of humans (Cusick, 2006; Saar & Novak, 2005). Sounds
are used for similar purposes and can result in symptoms such as ear pain,
anxiety, disorientation, and disrupted cognition (Brenner, 2010, p. 473).
Similarly, environmental factors such as light, human interaction, cage
cleaning, sound, and transport can all inuence well-being in animals
(Castelhano-Carlos & Baumans, 2009). Laboratory conditions can be noisy,
bright, and confusing to animals (Rollin & Kesel, 1995). Noises common
in human environments can be frightening to animals because of their
lack of familiarity and animals greater sensitivity to sound (Clough, 1982).
Ventilation systems, movement of equipment, human voices, vocalizations of
other animals, and the operation of equipment all contribute to the stressors
of the laboratory environment (Faith & Hessler, 2006). The effects of sound
on human and animal neuroendocrine, cardiovascular, and sleep functions
have been well documented. Loud noises can impair cardiovascular func-
tion, HPA axis regulation, hippocampal and memory encoding activity, and
amygdala activity (Brenner, 2010; Day, Nebel, Sasse, & Campeau, 2005;
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Journal of Trauma & Dissociation, 13:448468, 2012 457
Gregory, 2004). Sleep deprivation among humans and animals has been
found to increase the risk for impaired immunological, cardiovascular, and
cognitive performance (Caldwell & Redeker, 2005; Kales et al., 1984; N. L.
Rogers, Szuba, Staab, Evans, & Dinges, 2001). For example, sleep depriva-
tion has been found to cause hyperarousal in mice (Lopez-Rodriguez, Kim,
& Poland, 2004) and aggressive behavior, weight loss, and adverse changes
in physiological parameters in rats (Rechtschaffen & Bergmann, 2002; Webb,
1962). Sleep deprived mice and rabbits have demonstrated impairments in
immune function (Toth, 1995).
Threats to Physical Integrity and Life
Among human political prisoners and detainees, threats of death, mock exe-
cutions, exposure to extremes in temperature, connement to overly small
spaces, and injuries are common torture techniques that induce signicant
fear and anxiety (Brenner, 2010). Techniques such as water boarding can
result in feelings of helplessness and fear of death. Likewise, intentionally
exposing animals to predator threats (Cohen et al., 2006), placing them in
positions in which they will be subjected to aggressive behaviors by con-
specics (Van der Meer, Van Loo, & Baumans, 2004), provoking aggression,
or repeating procedures that have caused physical or psychological distress
in the past can cause animals to exhibit evidence of anticipatory anxiety
(Pfaff, 2002). In fact, foundational experiments that led to theories of learned
helplessness and clinical depression involved conditioning dogs and mice
with inescapable electric shocks (Seligman, 1972; Seligman & Maier, 1967).
Similar ndings have been described in other animals.
CASE STUDIES
We reviewed common animal research protocols to identify research condi-
tions that can contribute to pain, distress, and suffering. The cases reviewed
include the forced swim test commonly conducted with mice, spinal cord
injury experiments in cats, cardiac pacing studies in dogs, and toxicity
studies using monkeys. General details of these protocols are provided
here. Furthermore, we explore some of the experimental and incidental
harms associated with each research protocol, building upon the foundation
provided previously.
Mice: Forced Swim Test
A common research protocol that uses mice is the forced swim test (see
Figure 1). Although many of the primary symptoms of depression, such
as low self-esteem, guilt, and suicidal ideation, are difcult or impossible
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458 H. Ferdowsian and D. Merskin
FIGURE 1 Forced swim test.
to elicit from animals (Castagn, Moser, & Porsolt, 2009), the forced swim
test is commonly used in preclinical antidepressant efcacy screening
protocols (Petit-Demouliere, Chenu, & Bourin, 2004). This experimental
protocol is designed to demonstrate symptoms of depression, including
learned helplessness, in rodents. In the forced swim test (also known as the
behavioral despair test), mice are placed in containers of water of which
they cannot touch the bottom or from which they cannot escape. The time
rodents spend swimming, struggling, and oating is measured. Some mice
struggle throughout the entire scheduled session, whereas others eventually
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Journal of Trauma & Dissociation, 13:448468, 2012 459
become passive and oat, moving only enough to keep their eyes and
noses above water. Resignation (behavioral despair, learned helplessness) is
used as a primary behavioral parameter for antidepressant activity (Porsolt,
Brossard, Hautbois, & Roux, 2001). Periods of immobility are measured in
relationship to pharmaceutical intervention.
As a result of the forced swim test, researchers have reported profound
chronic changes in biological and behavioral parameters in rodents (Becker
et al., 2008). Behavioral despair, induced hyperactivity of the HPA axis, loss
of body weight, and hypothermia often occur after the stress of the proto-
col. The prolonged immobility of the forced swim test amplies feelings of
helplessness.
Cats: Spinalization
Cats are used in spinal cord injury experiments, in which they are anes-
thetized and intubated while a laminectomy is performed (Marcoux &
Rossignol, 2000). The cats spinal cords are then severed with surgical scis-
sors and an absorbable hemostat is placed to ll the space, followed by
suturing of the wound. The wounds remain partially open to reveal the
spinal cord, and S-hooks are attached through which pressure is admin-
istered to approximate weight-bearing loads. The cats awaken paralyzed.
After surgical intervention, the cats are placed in individual cages, with
daily interventions including manual bladder expression and cleaning of
their hindquarters.
Dogs: Ventricular Pacing
Dogs are used in ventricular pacing studies, in which their heart rates
are elevated for extended periods of time to approximate heart failure in
humans. Although the normal heart rate for adult dogs is 70120 beats per
minute, cardiac pacing protocols dictate rapid pacing from 130 to more than
600 beats per minute (Ahlberg, Ripplinger, Skadsberg, Iaizzo, & Mulligan,
2007; Everett et al., 2000; Khoury et al., 2009). Tachycardia is maintained, in
some cases for days and weeks at a time. Protocols include surgical inter-
vention, instrumentation, rapid atrial or ventricular pacing, pharmacological
intervention, and euthanasia. Cardiovascular consequences include severe
ventricular arrhythmias, changes in hemodynamic parameters (e.g., blood
pressure and vascular resistance), physiological changes (e.g., heart rate, car-
diac output, stroke volume, contractility and relaxation), and death (Ahlberg
et al., 2007; Everett et al., 2000; Khoury et al., 2009).
Monkeys: Toxicology Tests
Monkeys are commonly used in toxicity tests in order to estimate the poten-
tial effects in and risks to humans (Dorato & Buckley, 2006; Gad, 2009;
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460 H. Ferdowsian and D. Merskin
Grote-Wessels, Frings, Smith, & Weinbauer, 2009; Korte, Vogel, & Osterburg,
1987). A typical method for studying acute systemic toxicity among primates
is a pyramiding dosage design (Gad, 2009, p. 215). Drugs are administered
in escalating amounts via oral, intravenous, and pulmonary routes, including
gavage. Monkeys are exposed to the highest tolerable levels (Hayes, 2007,
p. 1608), although death, particularly in reproductive and developmental
toxicology studies, is not unusual (Buse, Habermann, Osterburg, Korte, &
Weinbauer, 2003; Martin & Weinbauer, 2010).
Monkey fetuses and infants are used to investigate drug effects on
organogenesis; toxic doses are typically administered to the mothers during
pregnancy or lactation. Mothers are captured from the wild or purposefully
bred, shipped, caged, and repeatedly handled in the laboratory. Their
offspring often abort or die early. If infants survive, they are typically taken
from their mothers shortly after birth. In one protocol, colony-bred adult
female rhesus monkeys were purchased from China for use in Japan, where
the monkeys were kept in stainless steel cages (Yasuda et al., 2005). Male
monkeys were housed with female monkeys on Days 12, 13, and 14 of the
female monkeys menstrual cycles in order to induce sexual intercourse and
pregnancy. Pregnancy was conrmed with ultrasound after monkeys were
anesthetized with ketamine. Subsequently, pregnant mothers were weighed
every 20 days and injected with varying dosage levels of dioxin. Once the
babies were delivered, they lived with their mothers for 1 year and were
exposed to dioxin through breast milk. The young monkeys were weighed
every 10 days, then euthanized, so researchers could examine morbidity
and mortality associated with dioxin exposure. Morbidity included severe
dental disease.
DISCUSSION
The examples presented here highlight research conditions that can con-
tribute to pain, distress, and suffering. In addition to the pain and distress
associated with experimental protocols, animals also experience pain,
distress, and suffering as a result of routine aspects of the laboratory
environment. Thwarted opportunities to fulll and express species-specic
behaviors can also result in suffering (Jensen & Toates, 1993; Rollin, 2010).
All of the cases described here include the potential for experimental
and incidental harms, such as severed bonds and social deprivation, isola-
tion and sensory deprivation, the inability to fulll natural behaviors, and
threats to animals physical integrity and lives. For example, mice used in
forced swim test protocols experience near-drowning and hypothermia as
well as sleep disruption and depression (which are goals of the experimen-
tal intervention), shipment, frequent handling and cage transfers, instrument
placement, and connement.
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Journal of Trauma & Dissociation, 13:448468, 2012 461
Likewise, spinal cord injury experiments expose cats to many of the
incidental harms incurred by mice in addition to life-threatening complica-
tions of spinal cord injury, including infection and shock. Cats are placed in
single-cage housing and prevented from fullling natural behaviors, lack
solitude and privacy, and are incapable of performing normal hygienic
practices.
Dogs also experience pain, distress, and suffering as a result of their use
in heart failure experiments. Like cats and mice, dogs are prevented from
forming normal bonds and engaging in normal socialization. Dogs experi-
ence threats to their physical integrity and lives (rapid ventricular pacing
and heart failure), overstimulation, disruption of natural sleep cycles, and
an inability to control or stop the pain and discomfort associated with the
protocol.
Monkeys also experience experimental and incidental harms as a result
of their use in toxicology experiments. Experimental harms include severe
pain and repeated threats to their physical integrity and lives. Incidental
harms include conditions of capture and breeding, maternal separation and
deprivation, isolation, and transport, among others. These monkeys and their
offspring are also unable to fulll natural behaviors such as socialization and
exploration.
CONCLUSIONS
Anatomical, physiological, and behavioral similarities across species demon-
strate that animals experience pain and distress in ways similar or identical to
humans. There are also commonalities in the factors that contribute to pain,
distress, and suffering in humans and other animals. Furthermore, animals
vulnerability and dependence on humans while in captivity likely contribute
to their suffering.
Although researchers can never be certain of the details of the expe-
riences of other animals, or even other humans, animals have necessary
and sufcient structures, systems, and mechanisms from which pain, dis-
tress, and suffering can occur. We have not exhausted the list of potential
harms to animals as a result of their use in laboratory research. Rather, our
goal was to consider and illustrate shared conditions of suffering among
humans and other animals. It is also worth noting that, just as human sur-
vivors react and recover in a range of ways, depending on their severity of
exposure, developmental level, support systems, coping mechanisms, and
recovery environment, so may animals in certain circumstances. Not all indi-
viduals experience long-term physical or psychological sequelae of trauma.
Nevertheless, it is the potential for physical and psychological trauma that
inevitably contributes to the ethical considerations regarding the use of ani-
mals in research. These ndings also have implications regarding other ways
in which animals are used by humans.
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REFERENCES
Recognition. (2009). Recognition and alleviation of pain in laboratory animals.
Washington, DC: Institute for Laboratory Animal Research.
Ahlberg, S. E., Ripplinger, C. M., Skadsberg, N. D., Iaizzo, P. A., & Mulligan, L.
(2007). Effects of pacing rate on mechanical restitution within the in vivo canine
heart: Study of the force-frequency relationship. Journal of Cardiovascular
Electrophysiology, 18, 212217.
Alleva, E., & Francia, N. (2009). Psychiatric vulnerability: Suggestions from animal
models and role of neurotrophins. Neuroscience & Biobehavioral Reviews, 33,
525536.
Andersen, H. S., Sestoft, D., Lillebaek, T., Gabrielsen, G., Hemmingsen, R., & Kramp,
P. (2000). A longitudinal study of prisoners on remand: Psychiatric prevalence,
incidence and psychopathology in solitary vs. non-solitary connement. Acta
Psychiatrica Scandinavia, 102, 1925.
Avgustinovich, D. F., & Kovalenko, I. L. (2005). Formation of behavioral pathol-
ogy in female C57BL/6J mice exposed to prolonged negative psychoemotional
conditions. Neuroscience and Behavioral Physiology, 35, 959967.
Balcombe, J. P., Barnard, N., & Sandusky, C. (2004). Laboratory routines cause
animal stress. Contemporary Topics in Laboratory Animal Science, 43(6), 4251.
Becker, C., Zeau, B., Rivat, C., Blugeot, A., Hamon, M., & Benoliel, J. J. (2008).
Repeated social defeat-induced depression-like behavioral and biological alter-
ations in rats: Involvement of cholecystokinin. Molecular Psychiatry, 12,
10791092.
Bellieni, C. V., & Buonocore, G. (2010). Recommendations for an ethical treatment
of newborns involved in clinical trials. Acta Paediatrica, 99(1), 3032.
Bentham, J. (1836). An introduction to the principles of morals and legislation.
London, England: Henry Frowde. (Original work published 1789)
Bloomsmith, M., Baker, K., Ross, S., & Pazol, K. (2002). The behavioural effects of
early rearing experience on captive chimpanzee behavioural development: The
juvenile years. American Journal of Primatology, 57(S1), 5455.
Bowen, J., & Heath, S. (2005). Behaviour problems in small animals: Practical
advice for the veterinary team. New York, NY: Elsevier Health Sciences.
Bowlby, J. (1969). Attachment and loss. Vol. 1: Attachment. London, England:
Hogarth.
Bowlby, J. (1973). Attachment and loss. Vol. 2: Separation: Anxiety and anger.
London, England: Hogarth.
Bowlby, J. (1980). Attachment and loss. Vol. 3: Loss: Sadness and depression.
London, England: Hogarth.
Bradshaw, G. A., Capaldo, T., Lindner, L., & Grow, G. (2008). Building an inner
sanctuary: Complex PTSD in chimpanzees. Journal of Trauma & Dissociation,
9, 934.
Brenner, G. H. (2010). The expected psychiatric impact of detention in Guantanamo
Bay, Cuba, and related considerations. Journal of Trauma & Dissociation, 11,
469487.
Broom, D. M. (2010). Cognitive ability and awareness in domestic animals and
decisions about obligations to animals. Applied Animal Behaviour Science, 126,
111.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

Journal of Trauma & Dissociation, 13:448468, 2012 463
Brne, M. (2008). Textbook of evolutionary psychiatry: The origins of
psychopathology. New York, NY: Oxford University Press.
Brne, M., Brne-Cohrs, U., McGrew, W. C., & Preuschoft, S. (2006).
Psychopathology in great apes: Concepts, treatment options and possible
homologies to human psychiatric disorders. Neuroscience and Behavioral
Reviews, 30, 12461259.
Buse, E., Habermann, G., Osterburg, I., Korte, R., & Weinbauer, G. F. (2003).
Reproductive/developmental toxicity and immunotoxicity assessment in the
nonhuman primate model. Toxicology, 221, 221227.
Caldwell, B. A., & Redeker, N. (2005). Sleep and trauma: An overview. Issues in
Mental Health Nursing, 26, 721738.
Callard, M. D., Bursten, S. N., & Price, E. O. (1999). Repetitive back ipping
behaviour in captive roof-rats (Rattus rattus) and the effect of cage enrichment.
Animal Welfare, 9, 139152.
Cantor, C., & Joyce, P. R. (2009). Evolution and psychiatry. Australian and New
Zealand Journal of Psychiatry, 43, 991993.
Carbone, L. (2004). What animals want: Expertise and advocacy in animal welfare
policy. New York, NY: Oxford University Press.
Cassell, E. J. (2004). The nature of suffering and the goals of medicine (2nd ed.).
New York, NY: Oxford University Press.
Castagn, V., Moser, P., & Porsolt, R. D. (2009). Behavioral assessment of antidepres-
sant activity in rodents. In J. J. Buccafusco (Ed.), Methods of behavior analysis
in neuroscience (2nd ed.). Boca Raton, FL: CRC Press. Retrieved from http://
www.ncbi.nlm.nih.gov/books/NBK5222/
Castelhano-Carlos, M. J., & Baumans, V. (2009). The impact of light, noise, cage
cleaning and in-house transport on welfare and stress of laboratory rats.
Laboratory Animals, 43(4), 311327.
Chamberlain, D. B. (1989). Babies remember pain. Pre- and Peri-Natal Psychology,
3(4), 297310.
Champoux, M., Metz, B., & Suomi, S. J. (1991). Behaviour of nursery/peer-reared
and mother-reared rhesus monkeys from birth through 2 years of age. Primates,
32, 509514.
Clough, G. (1982). Environmental effects on animals used in biomedical research.
Biological Review, 57, 487523.
Cohen, H., Matar, M. M., Richter-Levin, G., & Zohar, J. (2006). The contribution of
an animal model toward uncovering biological risk factors for PTSD. Annals of
the New York Academy of Sciences, 1071, 335350.
Cusick, S. G. (2006). Music as torture/music as weapon. Transcultural Music Review,
10. Retrieved from http://www.sibetrans.com/trans/trans10/cusick_eng.htm
Dantzer, R., & Kelley, K. W. (2007). Twenty years of research on cytokine-induced
sickness behavior. Brain, Behavior, and Immunity, 21(2), 153160.
Dawkins, M. S. (2008). The science of animal suffering. Ethology, 114, 937945.
Day, H. E., Nebel, S., Sasse, S., & Campeau, S. (2005). Inhibition of the central
extended amygdala by loud noise and restraint stress. European Journal of
Neuroscience, 21, 441454.
DeGrazia, D. (2002). Animal rights: A very short introduction. New York, NY: Oxford
University Press.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

464 H. Ferdowsian and D. Merskin
Dettling, A. C., Feldon, J., & Pryce, C. R. (2002). Repeated parental deprivation in
the infant common marmoset (Callithrix jacchus, primates) and analysis of its
effects on early development. Biological Psychiatry, 52, 10371046.
Dombrowski, D. A. (1997). Babies and beasts: The argument from marginal cases.
Chicago, IL: University of Illinois Press.
Dorato, M. A., & Buckley, L. A. (2006). Toxicology in the drug discovery and
development process. Current Protocols in Pharmacology, 10(3), 135.
Erwin, J. (1986). Environments for captive propagation of primates: Interaction of
social and physical factors. In K. W. Benirschke (Ed.), Primates: The road to
self-sustaining populations (pp. 297305). New York, NY: Springer-Verlag.
Everett, T. H., Li, H., Mangrum, J. M., McRury, I. D., Mitchell, M. A., Redick, J. A.,
& Haines, D. E. (2000). Electrical, morphological, and ultrastructural remod-
eling and reverse remodeling in a canine model of chronic atrial brillation.
Circulation, 102, 14541460.
Faith, R. E., & Hessler, J. (2006). Housing and environment. In M. A. Suckow, S. H.
Weisbroth, & C. L. Franklin (Eds.), The laboratory rat (pp. 303337). New York,
NY: Academic Press.
Ferdowsian, H., Durham, D., Kimwele, C., Kranendonk, G., Otali, E., Akugizibwe, T.,
. . . Johnson, C. M. (2011). Signs of mood and anxiety disorders in chimpanzees.
PLoS ONE 6(6), e19855. doi:10.1371/journal.pone.001985519855
Gad, S. C. (2009). Drug safety evaluation. New York, NY: Wiley.
Gregory, N. C. (2004). Physiology and behaviour of animal suffering. New York,
NY: Wiley.
Grote-Wessels, S., Frings, W., Smith, C. A., & Weinbauer, G. F. (2009).
Immunotoxicity in nonhuman primates. In R. R. Dietert (Ed.), Immunotoxicity
testing: Methods and protocols, methods in molecular biology (Vol. 598, pp.
341359). New York, NY: Springer.
Guyot, G. W., Bennett, T. L., & Cross, H. A. (1980). The effects of social isolation
on the behavior of juvenile domestic cats. Developmental Psychobiology, 13,
317329.
Guyot, G. W., Cross, H. A., & Bennett, T. L. (1980). Early social isolation of the
domestic cat: Responses to separation from social and nonsocial rearing stimuli.
Developmental Psychobiology, 13, 309315.
Harlow, H. F., Dodsworth, R. O., & Harlow, M. K. (1965). Total social isola-
tion in monkeys. Proceedings of the National Academy of Sciences, USA, 54,
9097.
Hayes, A. W. (2007). Principles and methods of toxicology. Boca Raton, FL: CRC
Press.
Hochner, B., Shomrat, T., & Fiorito, G. (2006). The octopus: A model for a com-
parative analysis of the evolution of learning and memory mechanisms. Marine
Biological Laboratory, 210, 308317.
IASP. (2007). IASP taxonomy. International Association for the Study of
Pain. Retrieved April 30, 2012, from http://www.iasp-pain.org/AM/Template.
cfm?Section=Pain_Denitions
Jensen, P., & Toates, F. M. (1993). Who needs behavioural needs? Motivational
aspects of the needs of animals. Applied Animal Behaviour Science, 37,
161181.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

Journal of Trauma & Dissociation, 13:448468, 2012 465
Kales, J., Kales, A., Bixler, M., Soldator, C., Cadoeix, R., Kashurba, G., & Vela-Bueno,
A. (1984). Biopsychobehavioral correlated of insomnia: Clinical characteristics
and behavioral correlates. American Journal of Psychiatry, 141, 13711376.
Khoury, D. S., Naware, M., Siou, J., Blomquist, A., Mathuria, N. S., Wang, J.,
. . . Panescu, D. (2009). Ambulatory monitoring of congestive heart failure
by multiple bioelectric impedance vectors. Journal of the American College of
Cardiology, 53, 10751081.
Kikusui, T., Isaka, Y., & Mori, Y. (2005). Early weaning deprives mouse pups of
maternal care and decreases their maternal behavior in adulthood. Behavioral
Brain Research, 162, 200206.
Kim, J., & Gorman, J. (2005). The psychobiology of anxiety. Clinical Neuroscience
Research, 4, 335347.
Korte, R., Vogel, F., & Osterburg, I. (1987). The primate model for hazard assessment
of teratogens in human. Archives of Toxicology Supplement, 11, 115121.
Kozorovitskiy, Y., Gross, C. G., Kopil, C., Battaglia, L., McBreen, M., Stranahan, A.
M., & Gould, E. (2005). Experience induces structural and biochemical changes
in the adult primate brain. Proceedings of the National Academy of Sciences,
USA, 102, 1747817482.
Lang, P. J., Davis, M., & Ohman, A. (2000). Fear and anxiety: Animal models and
human cognitive psychophysiology. Journal of Affective Disorders, 61, 137159.
Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt,
J. S., . . . Mogil, J. S. (2006, June 30). Social modulation of pain as evidence for
empathy in mice. Science, 312, 19671970.
Lariviere, W. R., & Mogil, J. S. (2010). The genetics of pain and analgesia in
laboratory animals. Methods in Molecular Biology, 617, 261278.
Latham, N. R., & Mason, G. J. (2004). From house mouse to mouse house: The
behavioural biology of free-living Mus musculus and its implications in the
laboratory. Applied Animal Behaviour Science, 86, 261289.
Latham, N. R., & Mason, G. J. (2008). Maternal deprivation and the development of
stereotypic behavior. Applied Animal Behaviour Science, 110, 84108.
Lautenbacher, S., Kundermann, B., & Krieg, J-C. (2006). Sleep deprivation and pain
perception. Sleep Medicine Reviews, 10, 357369.
Lopez-Rodriguez, F., Kim, J., & Poland, R. E. (2004). Total sleep deprivation
decreases immobility in the forced-swim test. Neuropsychopharmacology, 29,
11051111.
Lumpkin, E. A., & Bautista, D. M. (2005). Feeling the pressure in mammalian
somatosensation. Current Opinion in Neurobiology, 15(4), 382388.
Lutz, C., Well, A., & Novak, M. (2003). Stereotypic and self-injurious behavior in
rhesus macaques: A survey and retrospective analysis of environment and early
experience. American Journal of Primatology, 60, 115.
Marcoux, J., & Rossignol, S. (2000). Initiating or blocking locomotion in spinal
cats by noradrenergic drugs to restricted lumbar spinal segments. Journal of
Neuroscience, 20, 85778585.
Marino, L. (2002). Convergence of complex cognitive abilities in cetaceans and
primates. Brain, Behavior and Evolution, 59, 2132.
Martin, P. L., & Weinbauer, G. F. (2010). Developmental toxicity testing of biophar-
maceuticals in nonhuman primates: Previous experience and future directions.
International Journal of Toxicology, 29, 552568.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

466 H. Ferdowsian and D. Merskin
Mason, C. G. (Ed.). (2008). Stereotypic behaviour: Fundamentals and applications
to welfare. Wallingford, England: CABI.
Mather, J. A. (2008). Cephalopod consciousness: Behavioral evidence. Conscious
Cognition, 17, 3748.
McGowan, C. M., Stubbs, N., & Goff, L. (2007). Animal physiotherapy. New York,
NY: Wiley-Blackwell.
Merskey, H., & Bogduk, N. (1994). Classication of chronic pain. In H. Merskey &
N. Bogduk (Eds.), Descriptions of chronic pain syndromes and denitions of
pain terms (2nd ed., pp. 4043). Seattle, WA: IASP Press.
Moberg, G. P., & Mench, J. A. (2000). The biology of animal stress: Basic principles
and implications for animal welfare. Oxfordshire, England: CABI.
Morton, D. B., & Hau, J. (2002). Welfare assessment and humane endpoints. In J.
Hau & L. Van Hoosier, Jr. (Eds.), Handbook of laboratory animal science (Vol.
1, pp. 457486). Boca Raton, FL: CRC Press.
Murray, E. A. (2007). The amygdala, reward and emotion. Trends in Cognitive
Sciences, 2, 489497.
Newcomer, C. E. (2000). The history and histrionics of pain and dis-
tress in laboratory animals. Retrieved from http://www.nap.edu/openbook.
php?record_id=10035&page=87
Novak, M. A., Meyer, J. S., Lutz, C., & Tiefenbacher, S. (2006). Deprived envi-
ronments: Developmental insights from primatology. In G. J. Mason (Ed.),
Stereotypic behaviour: Fundamentals and applications to welfare (2d ed., pp.
153189). Wallingford, England: CABI.
Otani, S. (2004). Prefrontal cortex: From synaptic plasticity to cognition. Boston, MA:
Kluwer Academic.
Overall, K. L. (1994). Use of clomipramine to treat ritualistic motor behavior in dogs.
Journal of the American Veterinary Medical Association, 205, 17331741.
Overall, K. L. (2005). Veterinary behavioural medicine: A roadmap for the 21st
century. Veterinary Journal, 169, 130143.
Overall, K. L., & Dunham, A. E. (2002). Outcome of long-term treatment for
dogs with obsessive-compulsive disorder: Effects of age, breed, treatment
compliance, and co-morbidity. Journal of the American Veterinary Medical
Association, 221, 14451452.
Panksepp, J. (1982). Toward a general psychobiological theory of emotions.
Behavioral and Brain sciences, 5, 407468.
Panksepp, J. (1998). Affective neuroscience: The foundations of human and animal
emotions. New York, NY: Oxford University Press.
Panksepp, J. (2004). Affective neuroscience: The foundations of human and animal
emotions. New York, NY: Oxford University Press.
Panksepp, J., Herman, B., Conner, R., Bishop, P., & Scott, J. P. (1978). The biology of
social attachments: Opiates alleviate separation distress. Biological Psychiatry,
13, 607618.
Petit-Demouliere, B., Chenu, F., & Bourin, M. (2004). Forced swimming test in mice:
A review of antidepressant activity. Psychopharmacology, 177, 245255.
Pfaff, D. W. (2002). Hormones, brain, and behavior (Vol. 5). New York, NY: Elsevier.
Ploghaus, A., Tracey, I., Gati, J. S., Clare, S., Menon, R. S., Matthews, P. M., . . .
Rawlins, P. (1999, June 18). Dissociating pain from its anticipation in the human
brain. Science, 284, 19791981.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

Journal of Trauma & Dissociation, 13:448468, 2012 467
Pluhar, E. B. (1993). Arguing away suffering: The neo-Cartesian revival. Philosophy,
9(1), 2741.
Porsolt, R. D., Brossard, G., Hautbois, C., & Roux, S. (2001). Rodent models of
depression: Forced swimming and tail suspension behavioral despair tests in
rats and mice. Current Protocols in Neuroscience, Unit 8.10A, pp. 18.
Rechtschaffen, A., & Bergmann, B. M. (2002). Sleep deprivation in the rat: An update
of the 1989 paper. Sleep, 25, 1824.
Rogers, C. M., & Davenport, R. K. (1969). Effects of restricted rearing on sexual
behavior of chimpanzees. Developmental Psychology, 1, 200204.
Rogers, N. L., Szuba, M. P., Staab, J. P., Evans, D. L., & Dinges, D. F. (2001).
Neuroimmunologic aspects of sleep and sleep loss. Seminars in Clinical
Neuropsychiatry, 6, 295307.
Rollin, B. E. (2010). Why is agricultural animal welfare important? The social and
ethical context. In T. Grandin (Ed.), Improving animal welfare: A practical
approach (pp. 2131). Oxfordshire, England: CABI.
Rollin, B. E., & Kesel, M. L. (1995). The experimental animal in biomedical research:
Care, husbandry, and well being; an overview by species. Boca Raton, FL: CRC
Press.
Rolls, E. T. (2005). Emotions explained. New York, NY: Oxford University Press.
Saar, E., & Novak, V. (2005). Inside the wire: A military intelligence soldiers
eyewitness account of life at Guantanamo. New York, NY: Guilford Press.
Seligman, M. E. (1972). Learned helplessness. Annual Review of Medicine, 23,
407412.
Seligman, M. E. P., & Maier, S. F. (1967). Failure to escape traumatic shock. Journal
of Experimental Psychology, 74, 19.
Shettleworth, S. J. (1998). Cognition, evolution, and behavior. Oxford, England:
Oxford University Press.
Siegmund, A., & Wotjak, C. T. (2006). Towards an animal model of posttraumatic
stress disorder. Annals of the New York Academy of Science, 1071, 324334.
Singer, P. (2006). In defense of animals: The second wave. New York, NY: Wiley-
Blackwell.
Smith, C. P., & Taylor, V. (1996). Environmental enrichment information resources
for laboratory animals: 1965-1995. Darby, PA: Diane.
Stevens, A., & Price, J. (2000). Evolutionary psychiatry: A new beginning. London,
England: Routledge.
Strekalova, T., Spanagel, R., Bartsch, D., Henn, F., & Gass, P. (2004). Stress-
induced anhedonia in mice is associated with decits in forced swimming and
exploration. Neuropsychopharmacology, 29, 20072017.
Suedfeld, P., & Steel, D. G. (2000). The environmental psychology of capsule
habitats. Annual Review of Psychology, 51, 227253.
Tarr, B. A., Rabinowitz, J. S., Imtiaz, M. A., & DeVoogd, T. J. (2009). Captivity
reduces hippocampal volume but not survival of new cells in a food-storing
bird. Developmental Neurobiology, 69, 972981.
Toth, L. (1995). Immune-modulatory drugs alter Candid allucans-induced sleep
patterns in rabbits. Pharmacology Biochemistry Behavior, 51(4), 877884.
Van der Meer, E., Van Loo, P. L. P., & Baumans, V. (2004). Short-term effects of
a disturbed light dark cycle and environmental enrichment on aggression and
stress-related parameters in male mice. Laboratory Animal, 38, 376383.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
6
:
2
6

1
9

J
u
n
e

2
0
1
2

468 H. Ferdowsian and D. Merskin
Waiblinger, E., & Konig, B. (2004). Renement of gerbil housing and husbandry in
the lab. Alternatives to Laboratory Animals, 32, 163169.
Webb, W. B. (1962). Some effects of prolonged sleep deprivation on the hooded
rat. Journal of Comparative Physiological Psychology, 55, 791793.
Wrbel, H., & Stauffacher, M. (1997). Age and weight at weaning affects corticos-
terone levels and development of stereotypies in ICR mice. Animal Behavior,
53, 891900.
Yasuda, I., Yasuda, M., Sumida, H., Tsusaki, H., Arima, A., Ihara, T., . . . Akagawa, Y.
(2005). In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin
affects tooth development in rhesus monkeys. Reproductive Toxicology, 20(1),
2130.
Zimmermann, M. (1986). Behavioral investigations of pain in animals. In I. J. H.
Duncan & V. Molony (Eds.), Assessing pain in farm animals (pp. 1629).
Luxembourg: Ofce for Ofcial Publications of the European Communities.
D
o
w
n
l
o
a
d
e
d

b
y

[
U
n
i
v
e
r
s
i
t
y

o
f

O
r
e
g
o
n
]

a
t

1
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1
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