Parallels in Suffering

8/12/2019 Parallels in Suffering

1/22

This article was downloaded by: [University of Oregon]On: 19 June 2012, At: 16:26Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Journal of Trauma & DissociationPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/wjtd20

Parallels in Sources of Trauma, Pain,Distress, and Suffering in Humans andNonhuman AnimalsHope Ferdowsian MDMPH a & Debra Merskin PhD ba

Physician's Committee for Responsible Medicine; Department of Medicine, George Washington University, Washington, DC, USAb 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 Sourcesof Trauma, Pain, Distress, and Suffering in Humans and Nonhuman Animals, Journal of Trauma &

Dissociation, 13:4, 448-468To link to this article: http://dx.doi.org/10.1080/15299732.2011.652346

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Anysubstantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,systematic supply, or distribution in any form to anyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representationthat the contents will be complete or accurate or up to date. The accuracy of anyinstructions, formulae, and drug doses should be independently verified with primarysources. The publisher shall not be liable for any loss, actions, claims, proceedings,demand, or costs or damages wha tsoever or howsoever caused arising directly orindirectly in connection with or arising out of the use of this material.
http://www.tandfonline.com/loi/wjtd20http://www.tandfonline.com/page/terms-and-conditionshttp://dx.doi.org/10.1080/15299732.2011.652346http://www.tandfonline.com/loi/wjtd20


2/22

Journal of Trauma & Dissociation , 13:448468, 2012Copyright Taylor & Francis Group, LLCISSN: 1529-9732 print/1529-9740 onlineDOI: 10.1080/15299732.2011.652346

Parallels in Sources of Trauma, Pain,Distress, and Suffering in Humansand Nonhuman Animals

HOPE FERDOWSIAN, MD, MPH Physicians Committee for Responsible Medicine; Department of Medicine, George

Washington University, Washington, DC, USA

DEBRA MERSKIN, PhDSchool 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 commonanimal 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: [email protected]

448

D

w

U

O


3/22

Journal of Trauma & Dissociation , 13:448468, 2012 449

interventions to minimize pain and distress in animals commonly focus onreducing the numbers of animals used and making changes to specic pro-tocols rather than evaluating the suffering individual animals experienceover 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 usedin research, there is an ethical imperative to better understand the cumulativeeffects of captivity and the rigors of laboratory research on animals.

In 1789, moral philosopher and legal scholar Jeremy Bentham notedthat it is the ability to suffer, not the ability to reason, that should be theinsuperable line (1789 / 1836, p. 236) that determines the treatment of otherbeings, including infants, adults with particular disabilities, and animals. According to Bentham,

A full-grown horse or dog is beyond comparison a more rational, as wellas a more conversable animal, than an infant of a day or a week or evena 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 andother animals has evolved signicantly since Benthams statement was rstpublished. Only in relatively recent history have scientists and physiciansacknowledged that human infants experience pain (Bellieni & Buonocore,2010; Chamberlain, 1989). Furthermore, some have suggested that babiesand 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, andthe inability to communicate verbally does not negate the possibility that anindividual is experiencing pain (Merskey & Bogduk, 1994, p. 211). Althoughthis statement was intended to apply to infants and other humans unable toarticulate 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 isunknown, 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 unpleasantsubjective 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

D

w

U

O


4/22

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 andphysiological parameters. Suffering can be dened as a set of negative emo-

tions such as fear and pain and recognized operationally as states causedby negative reinforcers (Dawkins, 2008). Thus, suffering can manifest asphysical 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 centralquestions, we review anatomical, physiological, and behavioral similaritiesbetween 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 alsoexplore 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 humansand existing laboratory conditions for animals. Finally, we examine four casestudies of common animal research protocols in order to illustrate researchconditions 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 frommultiple disciplines provide objective evidence of animals abilities to expe-rience pain. In fact, much of what experts understand about animal painstems from studies in which animals were intentionally exposed to painfulor distressful experiences.

Partially as a result of homologous anatomical structures and physio-logical mechanisms, animals demonstrate coordinated responses to pain andmany emotional states and responses that are similar to those of humans. As dened by the International Association for the Study of Pain (2007), painis an unpleasant sensory and emotional experience associated with actualor potential tissue damage, or described in terms of such damage (p. 1979).In its specic application to animals, Zimmermann (1986, p. 16) modiedthe denition to include an aversive sensory experience caused by actual orpotential injury that elicits progressive motor and vegetative reactions, resultsin learned avoidance behavior, and may modify species-specic behavior,

including social behavior.

D

w

U

O


5/22


Anatomical and Physiological SimilaritiesIn vertebrates, pain and proprioception are mediated by somatosensory neurons of the trigeminal and dorsal root ganglia, which terminate in theskin and other tissues. Somatosensory stimuli trigger electrical impulses thatare 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 nervoussystems 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 thecerebral 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 canexplain similarities and differences in emotional processes across speciesby the ways in which humans and animals have adapted to different eco-logical niches (Shettleworth, 1998). Analgesics can modify pain responsesin animals as they do in humans. Pain may result in physiological changesinvolving the heart, kidneys, immune system, and other organ systems thatare critical to disease progression and recovery (Gregory, 2004). Animals canexperience acute or immediate pain, as well as slow crescendo pain, such asthe pain of inammation, visceral pain, and neuropathic pain. Although thenociceptive pathways of pain are fairly well described, the molecular mech-

anisms involved in pain perception and the neurological responses to tissueand neuronal injury are not well understood in humans or other animals.This complicates the ability to adequately prevent, recognize, and treat painin 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, sleepdisturbances, and enhanced sensitivity to pain (Dantzer & Kelley, 2007).Cytokines have sickness-inducing properties, partly as a result of the activation of the hypothalamicpituitaryadrenal (HPA) axis. Sickness behavioroccurs in mammals and birds (Dantzer & Kelley, 2007), and it is now under-stood that communication systems that link the immune and central nervoussystems, 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 formsof pain, and sensitivity to pain and pain-related traits may in part be heri-table (Lariviere & Mogil, 2010). Factors such as sleep deprivation have alsobeen associated with pain perception, although the direction of causality issometimes unclear (Lautenbacher, Kundermann, & Krieg, 2006). In additionto individual differences, other physical and psychological stressors can

D

w

U

O


6/22


contribute signicantly to the perception of pain as well as to an individualsability to cope with pain.

Behavioral Similarities Animals express pain in ways similar to humans, including throughavoidance behaviors, abnormal postures, guarding to protect an affectedarea, vocalizations such as whimpering, aggression, and physiological andendocrine responses, among others (Gregory, 2004). Furthermore, the antic-ipation of pain can result in mood and behavioral changes that exacerbatepsychological distress (Ploghaus et al., 1999).

Behavioral observations have been important in ascertaining whenand how animals experience pain. However, just as there are variationsin the expression of suffering within human populations, there are alsodifferences across species and between individual animals. Because of evo-lutionary pressures, some animals may be more likely than others to usecertain response behaviors. For example, many animals develop mecha-nisms that suppress signs of acute and chronic pain, particularly during timesof extreme fear (Gregory, 2004; McGowan, Stubbs, & Goff, 2007). Animals vulnerable to predation may attempt to hide signs of pain in attempts toenhance survival (Moberg & Mench, 2000) but may experience psychologicalsequelae. 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 functionare guided by genetic factors, environment and experiences help shapebrain 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 sharedacross 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 acommon 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 withless organized neural circuits may demonstrate less exibility and have more

limited coping mechanisms. Some animals may suffer more than humans

D

w

U

O


7/22


would in an analogous situation because of their inability to understand what is happening to them, make sense of their plight, escape from it, oralter their conditions.

Mammals share a large number of brain regions associated with emo-

tional affect, including the amygdala, hippocampus, hypothalamus, andprefrontal 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 persistentdisorders of social behavior (Brne, 2008). For example, fear responses arestored as memories and linked to the amygdala and can be expressed inmammals 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 changesto 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 identiedin animals who have been conned, restrained, or isolated and after sur-gical procedures (Gregory, 2004). Moreover, studies have indicated thathypothalamic 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 acrossspecies. 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 andincreases in sensitized fear related to hyperarousal, emotional blunting, andsocial withdrawal, as seen in posttraumatic stress disorder (Siegmund &

Wotjak, 2006). A study of juvenile rats designed to model childhood traumafound that exposing the rats to litter soaked in predator (cat) urine increasedthe likelihood that they would develop long-term behavioral disruptionsthought to represent posttraumatic stress symptom equivalents. When therats 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

D

w

U

O


8/22


empathic responses when painful stimuli are inicted on individuals they know (Langford et al., 2006).

THE EFFECTS OF CAPTIVITY AND LABORATORY CONDITIONSPain and distress are commonly experienced in the laboratory as a resultof experimental protocols or incidentally (Balcombe, Barnard, & Sandusky,2004; Carbone, 2004; Newcomer, 2000; Panksepp, 2004). Potential sourcesof pain and distress are present from birth (or even the prenatal period) todeath and can include birth conditions, maternal separation, connement,cage transfers, handling, painful procedures, social isolation, restraint, anddeprivation of simple needs (e.g., adequate sleep, food, water, and shel-ter). For use in research, animals are regularly transported from a breedingfacility or natural habitat to a laboratory. Animals also experience socialdeprivation, 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 factorsresemble potentially traumatic conditions and consequences of human cap-tivity that have been described elsewhere (Brenner, 2010). Here we exploreparallels between traumatic conditions for humans and common laboratory conditions for animals and explore the similar pathologies resulting fromthese conditions. Table 1 also illustrates cross-species parallels regarding thepotential 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 socialpressures

Withholding of adequate nutrition Isolation or inability to seek solitudeInadequate provision of shelter, sanitation,

and hygieneSensory deprivation or overstimulation

Restriction of physical activity or exercise Deprivation of the ability to fulllnatural behaviors or loss of autonomy

Invasive procedures, including sharp andblunt trauma, burns, induced diseases,unnecessary surgical procedures, andforms of death

Threats to physical integrity or threatsof death

Withholding of adequate health care Witnessing of painful or distressfulprocedures

D

w

U

O


9/22


social support and development. Among both humans and animals, if a par-ent is not present early in life, offspring are likely to develop stereotypicbehaviors (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 caseif they were free living (Latham & Mason, 2008). Interruption in maternalcare, or restricted access to mothers who are sometimes less able to carefor 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 mothersat 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 asa 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). Prematureseparation from mothers also leads to a range of adverse behavioral andsocial 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 behaviorshave 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 forpsychopathology, including symptoms of depression and anxiety (Andersenet al., 2000; Brenner, 2010). Even in conditions in which they choose to be ina temporarily isolating environment, such as polar expeditions, individualsfrequently experience depression, anxiety, paranoia, and physical symptomssuch 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

D

w

U

O


10/22


inherently social but are frequently kept under conditions of prolonged iso-lation and sensory deprivation. As a result, animals can exhibit abnormalbehaviors such as whole-body stereotypies and self-mutilation, which canbe 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 androdents brain regions (Kozorovitskiy et al., 2005) important to memory, suchas the hippocampus.

Isolation and lack of social stimulation can contribute to distress, par-ticularly among animals whose natural behaviors are highly social andinvolve seeking and play (Smith & Taylor, 1996). For example, tail biting,stereotypies, and neurotic behaviors are often exhibited in pigs withoutaccess 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 alsoexhibit 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, andimpulse control, often appear in the rst few years of life when neuralsystems are maturing (Overall, 1994, 2005; Overall & Dunham, 2002).

Sensory Overstimulation, Sleep Deprivation, and Circadian CycleDisruptionExposure to orescent light and disruption of sleep cycles are typical toolsin the interrogation of humans (Cusick, 2006; Saar & Novak, 2005). Soundsare 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, cagecleaning, 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 commonin human environments can be frightening to animals because of theirlack 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 stressorsof the laboratory environment (Faith & Hessler, 2006). The effects of soundon human and animal neuroendocrine, cardiovascular, and sleep functionshave 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;

D

w

U

O


11/22


Gregory, 2004). Sleep deprivation among humans and animals has beenfound to increase the risk for impaired immunological, cardiovascular, andcognitive 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 changesin physiological parameters in rats (Rechtschaffen & Bergmann, 2002; Webb,1962). Sleep deprived mice and rabbits have demonstrated impairments inimmune 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 smallspaces, and injuries are common torture techniques that induce signicantfear and anxiety (Brenner, 2010). Techniques such as water boarding canresult in feelings of helplessness and fear of death. Likewise, intentionally exposing animals to predator threats (Cohen et al., 2006), placing them inpositions 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 distressin the past can cause animals to exhibit evidence of anticipatory anxiety (Pfaff, 2002). In fact, foundational experiments that led to theories of learnedhelplessness 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 reviewedinclude 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 providedhere. Furthermore, we explore some of the experimental and incidentalharms associated with each research protocol, building upon the foundationprovided previously.

Mice: Forced Swim Test A common research protocol that uses mice is the forced swim test (seeFigure 1). Although many of the primary symptoms of depression, such

as low self-esteem, guilt, and suicidal ideation, are difcult or impossible

D

w

U

O


12/22


FIGURE 1 Forced swim test.

to elicit from animals (Castagn, Moser, & Porsolt, 2009), the forced swimtest is commonly used in preclinical antidepressant efcacy screeningprotocols (Petit-Demouliere, Chenu, & Bourin, 2004). This experimentalprotocol is designed to demonstrate symptoms of depression, includinglearned helplessness, in rodents. In the forced swim test (also known as thebehavioral despair test ), mice are placed in containers of water of whichthey cannot touch the bottom or from which they cannot escape. The time

rodents spend swimming, struggling, and oating is measured. Some micestruggle throughout the entire scheduled session, whereas others eventually

D

w

U

O


13/22


become passive and oat, moving only enough to keep their eyes andnoses above water. Resignation (behavioral despair, learned helplessness) isused 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 profoundchronic changes in biological and behavioral parameters in rodents (Beckeret al., 2008). Behavioral despair, induced hyperactivity of the HPA axis, lossof 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 thespinal 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, withdaily interventions including manual bladder expression and cleaning of their hindquarters.

Dogs: Ventricular PacingDogs are used in ventricular pacing studies, in which their heart ratesare elevated for extended periods of time to approximate heart failure inhumans. Although the normal heart rate for adult dogs is 70120 beats perminute, cardiac pacing protocols dictate rapid pacing from 130 to more than600 beats per minute (Ahlberg, Ripplinger, Skadsberg, Iaizzo, & Mulligan,2007; Everett et al., 2000; Khoury et al., 2009). Tachycardia is maintained, insome cases for days and weeks at a time. Protocols include surgical intervention, instrumentation, rapid atrial or ventricular pacing, pharmacologicalintervention, and euthanasia. Cardiovascular consequences include severe ventricular arrhythmias, changes in hemodynamic parameters (e.g., bloodpressure and vascular resistance), physiological changes (e.g., heart rate, car-diac output, stroke volume, contractility and relaxation), and death (Ahlberget 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;

D

w

U

O


14/22


Grote-Wessels, Frings, Smith, & Weinbauer, 2009; Korte, Vogel, & Osterburg,1987). A typical method for studying acute systemic toxicity among primatesis a pyramiding dosage design (Gad, 2009, p. 215). Drugs are administeredin 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 developmentaltoxicology studies, is not unusual (Buse, Habermann, Osterburg, Korte, & Weinbauer, 2003; Martin & Weinbauer, 2010).

Monkey fetuses and infants are used to investigate drug effects onorganogenesis; toxic doses are typically administered to the mothers duringpregnancy or lactation. Mothers are captured from the wild or purposefully bred, shipped, caged, and repeatedly handled in the laboratory. Theiroffspring often abort or die early. If infants survive, they are typically takenfrom their mothers shortly after birth. In one protocol, colony-bred adult

female rhesus monkeys were purchased from China for use in Japan, wherethe monkeys were kept in stainless steel cages (Yasuda et al., 2005). Malemonkeys were housed with female monkeys on Days 12, 13, and 14 of thefemale monkeys menstrual cycles in order to induce sexual intercourse andpregnancy. Pregnancy was conrmed with ultrasound after monkeys wereanesthetized with ketamine. Subsequently, pregnant mothers were weighedevery 20 days and injected with varying dosage levels of dioxin. Once thebabies were delivered, they lived with their mothers for 1 year and wereexposed to dioxin through breast milk. The young monkeys were weighedevery 10 days, then euthanized, so researchers could examine morbidity and mortality associated with dioxin exposure. Morbidity included severedental disease.

DISCUSSION

The examples presented here highlight research conditions that can con-tribute to pain, distress, and suffering. In addition to the pain and distressassociated 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-specicbehaviors can also result in suffering (Jensen & Toates, 1993; Rollin, 2010).

All of the cases described here include the potential for experimentaland incidental harms, such as severed bonds and social deprivation, isola-tion and sensory deprivation, the inability to fulll natural behaviors, andthreats to animals physical integrity and lives. For example, mice used inforced 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.

D

w

U

O


15/22


Likewise, spinal cord injury experiments expose cats to many of theincidental harms incurred by mice in addition to life-threatening complica-tions of spinal cord injury, including infection and shock. Cats are placed insingle-cage housing and prevented from fullling natural behaviors, lack

solitude and privacy, and are incapable of performing normal hygienicpractices.Dogs also experience pain, distress, and suffering as a result of their use

in heart failure experiments. Like cats and mice, dogs are prevented fromforming normal bonds and engaging in normal socialization. Dogs experi-ence threats to their physical integrity and lives (rapid ventricular pacingand heart failure), overstimulation, disruption of natural sleep cycles, andan inability to control or stop the pain and discomfort associated with theprotocol.

Monkeys also experience experimental and incidental harms as a result

of their use in toxicology experiments. Experimental harms include severepain and repeated threats to their physical integrity and lives. Incidentalharms include conditions of capture and breeding, maternal separation anddeprivation, isolation, and transport, among others. These monkeys and theiroffspring are also unable to fulll natural behaviors such as socialization andexploration.

CONCLUSIONS

Anatomical, physiological, and behavioral similarities across species demon-strate that animals experience pain and distress in ways similar or identical tohumans. 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 contributeto 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, ourgoal was to consider and illustrate shared conditions of suffering amonghumans 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, andrecovery environment, so may animals in certain circumstances. Not all individuals experience long-term physical or psychological sequelae of trauma.Nevertheless, it is the potential for physical and psychological trauma thatinevitably contributes to the ethical considerations regarding the use of ani-mals in research. These ndings also have implications regarding other waysin which animals are used by humans.

D

w

U

O


16/22


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 canineheart: Study of the force-frequency relationship. Journal of Cardiovascular Electrophysiology , 18 , 212217.

Alleva, E., & Francia, N. (2009). Psychiatric vulnerability: Suggestions from animalmodels 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 psychoemotionalconditions. Neuroscience and Behavioral Physiology , 35 , 959967.

Balcombe, J. P., Barnard, N., & Sandusky, C. (2004). Laboratory routines causeanimal 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 treatmentof 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: Thejuvenile 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 GuantanamoBay, Cuba, and related considerations. Journal of Trauma & Dissociation , 11 ,469487.

Broom, D. M. (2010). Cognitive ability and awareness in domestic animals anddecisions about obligations to animals. Applied Animal Behaviour Science , 126 ,111.

D

w

U

O


17/22


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 possiblehomologies 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 thenonhuman 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 ippingbehaviour 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, cagecleaning 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-rearedand 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-inducedsickness 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: OxfordUniversity Press.

D

w

U

O


18/22


Dettling, A. C., Feldon, J., & Pryce, C. R. (2002). Repeated parental deprivation inthe infant common marmoset ( Callithrix jacchus , primates) and analysis of itseffects 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 anddevelopment 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 isolationon the behavior of juvenile domestic cats. Developmental Psychobiology , 13 ,317329.

Guyot, G. W., Cross, H. A., & Bennett, T. L. (1980). Early social isolation of thedomestic 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: CRCPress.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? Motivationalaspects of the needs of animals. Applied Animal Behaviour Science , 37 ,161181.

D

w

U

O


19/22


Kales, J., Kales, A., Bixler, M., Soldator, C., Cadoeix, R., Kashurba, G., & Vela-Bueno, A. (1984). Biopsychobehavioral correlated of insomnia: Clinical characteristicsand 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 failureby 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 assessmentof 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 changesin 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 andhuman 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 forempathy in mice. Science , 312 , 19671970.

Lariviere, W. R., & Mogil, J. S. (2010). The genetics of pain and analgesia inlaboratory animals. Methods in Molecular Biology , 617 , 261278.

Latham, N. R., & Mason, G. J. (2004). From house mouse to mouse house: Thebehavioural biology of free-living Mus musculus and its implications in thelaboratory. 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 painperception. Sleep Medicine Reviews , 10 , 357369.

Lopez-Rodriguez, F., Kim, J., & Poland, R. E. (2004). Total sleep deprivationdecreases 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 inrhesus 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 spinalcats by noradrenergic drugs to restricted lumbar spinal segments. Journal of Neuroscience , 20 , 85778585.

Marino, L. (2002). Convergence of complex cognitive abilities in cetaceans andprimates. 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

w

U

O


20/22


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 21stcentury. Veterinary Journal , 169 , 130143.

Overall, K. L., & Dunham, A. E. (2002). Outcome of long-term treatment fordogs with obsessive-compulsive disorder: Effects of age, breed, treatmentcompliance, 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 humanbrain. Science , 284 , 19791981.

D

w

U

O


21/22


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 inrats and mice. Current Protocols in Neuroscience , Unit 8.10A, pp. 18.

Rechtschaffen, A., & Bergmann, B. M. (2002). Sleep deprivation in the rat: An updateof the 1989 paper. Sleep, 25 , 1824.

Rogers, C. M., & Davenport, R. K. (1969). Effects of restricted rearing on sexualbehavior 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 andethical 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: CRCPress.

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 andexploration. 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-storingbird. Developmental Neurobiology , 69 , 972981.

Toth, L. (1995). Immune-modulatory drugs alter Candid allucans -induced sleeppatterns 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 andstress-related parameters in male mice. Laboratory Animal , 38 , 376383.

D

w

U

O


22/22


Waiblinger, E., & Konig, B. (2004). Renement of gerbil housing and husbandry inthe lab. Alternatives to Laboratory Animals , 32 , 163169.

Webb, W. B. (1962). Some effects of prolonged sleep deprivation on the hoodedrat. 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-dioxinaffects 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

w

U

O

Documents

Parallels in Suffering