Fear of noises affects canine problem solving behavior and locomotion in standardized cognitive tests
Introduction
Distressed reactions to noise, ranging from alterations in attentiveness through fears and phobias, are common pathological behavioral conditions in pet dogs. Many surveys report that up to 50% of dogs may be affected by some extreme reaction to some noise during their lifetime (Blackshaw et al., 1990; Dale et al., 2010; Blackwell et al., 2013; Storengen and Lingaas, 2015; Tiira and Lohi, 2015, 2016). True prevalence levels are unknown for any population (although see Dinwoodie et al., 2019). Reactions are most commonly reported for storms, fireworks and guns, but noises associated with vehicles, machines, alarms, et cetera can also trigger fearful, anxious or phobic responses in dogs (McCobb et al., 2001; King et al., 2003; Ley et al., 2007).
A number of terms are often used to describe an adverse reactive, fearful or phobic response, including noise aversion, noise fear, noise stress, storm or thunderstorm phobia and noise sensitivity. Criteria for labeling a dog ‘noise reactive’ or ‘phobic’ or any of these other terms are not usually included in most studies (but see Overall et al., 2001; Dreschel and Granger, 2005; Overall et al., 2016; Scheifele et al., 2016), nor are the range of behaviors potentially displayed by the afflicted dog often noted (but see Overall et al., 2001; Crowell-Davis et al., 2003; Tiira and Lohi, 2014, 2016; Overall et al., 2016). Diagnostic criteria require that noise phobic dogs exhibit a profound, non-graded, extreme response to noise, manifest as intense avoidance, escape, or anxiety and associated with the sympathetic branch of the autonomic nervous system (Overall et al., 2001). Dogs who are continuously and characteristically distressed when exposed to specified noises, including storms, but who do not meet the criteria for a ‘phobia’ may be classified as ‘reactive’ (Overall, 2013) or ‘sensitive’ (Sherman and Mills, 2008; Tiira and Lohi, 2016; Franzini de Souza et al., 2018; Lopes Fagundes et al., 2018).
Confusingly, ‘noise sensitivity’ is defined differently both in audiology and in human medicine/psychiatry. In audiology, ‘noise sensitivity’ is commonly used to describe the range of upper and lower limits of auditory capability (a sensitivity to certain frequencies and volume ranges of sounds), and often refers to hyperacusis (Eggermont, 2013). ‘Noise sensitivity’ has also been defined in human ‘annoyance’ contexts: sensitivity to annoyance (expression of more annoyance than those around you for any given level of noise) and general susceptibility to noise (annoyance over a wide range of noises). In human psychiatry, the term ‘noise sensitivity’ has been used to characterize a relatively stable personality trait, independent of noise exposure (Belojevic et al., 2003; Stansfeld, 1996; Stansfeld et al., 1985, 2000; Milenković and Paunović, 2015).
We lack data to support any of these definitions for ‘noise sensitivity’ in dogs, so for those individuals who do not meet the diagnostic criteria for phobia, we have chosen to use the term ‘noise reactive’, which implies no underlying mechanism. This decision acknowledges that multiple underlying mechanisms may be contributory to the pathology, and uses ‘reactive’ within the context it is commonly used in experimental psychology and psychiatry to reflect a range of responses to a number of stimuli, which is applicable here (Epstein et al., 1978; Siniscalchi et al., 2013).
The behavioral signs of distress associated with noise reactivity and phobia may include trembling, freezing, panting, social withdrawal, pacing, salivating, urinating, defecating, destruction (with or without self-injury), hiding/crouching and escape/running away behaviors (Shull-Selcer and Stagg, 1991; Beerda et al., 1997, 1998; Overall et al., 2001; Crowell-Davis et al., 2003; Hydbring-Sandberg et al., 2004; Sherman and Mills, 2008; Sheppard and Mills, 2003; Tiira and Lohi, 2016), which are all classic responses to anxious states.
Noise stress (105 dB SPL) has been shown to impair higher order, pre-frontal cortex, delayed–response performance in cognitive trials in monkeys (Arnsten and Goldman-Rakic, 1998). Exposure to acute or chronic noise, itself, can distract from cognitive tasks (Söderlund et al., 2010). Noise reactivity and phobia interferes with performance in working dogs (Tomkins et al., 2011, 2012; Gazzano et al., 2007; Batt et al., 2008; Asher et al., 2013; Arvelius et al., 2014; Sherman et al., 2014; Evans et al., 2015), and interferes routine patterns of daily life in pet dogs (Overall et al., 2001, 2016).
We asked whether noise-reactivity, as scored from client reports using a standardized, validated questionnaire (Working Dog Questionnaire – PET version; WDQ-PET), was reflected in performance on the puzzle box test, one of 13 tests (Canine Intelligence Test Protocol; CITP) we used to evaluate the 4 commonly recognized cognitive domains (Social learning; Spatial learning/memory; Executive function/sustained attention/perseverance/inhibition; Spontaneous behavior (Lezak et al., 2004; Strauss et al., 2006; Gabowitz et al., 2008)). We also evaluated whether client reports and calculated Anxiety Intensity Rank (AIR) scores matched behavioral responses during a test using a custom designed 3.5 min noise recording. We hypothesized that reactivity to noise would adversely affect the puzzle box and noise test performance, and that client evaluations would contain false negatives, but no false positives, as has been shown elsewhere (Overall et al., 2016; Bellamy et al., 2018).
Section snippets
Study design
We reported on the pet dogs used in this study in an earlier paper where we asked whether auditory function, including auditory middle-latency response (AMLR), a measure of higher order cortical function, differed between dogs that were affected with noise reactivity and those that were not (Scheifele et al., 2016). These dogs were participants in a large study comparing problem solving ability of working dogs to that of pet dogs.
All dogs in all studies were assessed using either the Working
Analysis of AIR scores for dogs with auditory testing
Of the 35 dogs recruited from dogs already tested with the CITP, 22 were identified by clients completing the WDQ-PET as noise reactive and 13 were not. Of the 22 that were classified as noise reactive, 2 clients had said that their dogs did not react to noise upon enrollment but changed their minds once they completed the WDQ-PET with the detailed categories used to calculate AIR scores.
Of the 22 original noise reactive dogs, 5 were behaviorally too reactive to start or complete the auditory
Discussion
Problem solving ability is known to be affected by anxiety and fear. In dogs, separation anxiety/separation-related distress has been correlated with a negative cognitive bias (Mendl et al., 2010), and clinical anxieties have been shown to impair performance on solvable and insolvable tests (Passalacqua, Marshall-Pescini et al., 2013). The effects of noise, itself, may be important and somewhat separate from general fear. Noise reactivity affects the presentation of clinical signs of other
Conclusions
We compared noise reactive and non-reactive dogs with respect to AIR scores calculated from the WDQ-PET, reaction to a provocative noise recording, accelerometry and performance in a puzzle box test. There was an important association between performance on the noise section of the WDQ-PET and pattern/dimensions of movement as measured accelerometry. Movement across all aspects of the tests for noise reactive/phobic dogs was, on average, more erratic, subject to more starts and stops, and had
Acknowledgements
We thank Hope Veterinary Specialists in Malvern, PA, USA for renting us a large, open research space and for facilitating the study of the pet dogs. We thank Jess Lydon, CVT for her dedicated and extremely competent technical help. Special thanks are owed to Ali Brown and Leslie McDevitt who distributed the advertisement, the DTCCC (especially Sabine Platten) who reached out into the training community, and the 186 owners who volunteered > 150 dogs within 48 h, and the >100 incredible owners
References (64)
- et al.
A standardized behavior test for potential guide dog puppies: methods and association with subsequent success in guide dog training
J. Vet. Behav.
(2013) - et al.
Acute noise stress impairs feedback processing
Biol. Psychol.
(2012) - et al.
Factors associated with success in guide dog training
J. Vet. Behav.
(2008) - et al.
Manifestations of chronic and acute stress in dogs
Appl. Anim. Behav. Sci.
(1997) - et al.
Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs
Appl. Anim. Behav. Sci.
(1998) - et al.
DRD2 is associated with fear in some dog breeds
J. Vet. Behav.
(2018) - et al.
Aversive responses of dogs to ultrasonic, sonic and flashing light units
Appl. Anim. Behav. Sci.
(1990) - et al.
Fear responses to noises in domestic dogs: prevalence, risk factors and co-occurrence with other fear related behaviour
Appl. Anim. Behav. Sci.
(2013) - et al.
Roles for referential focus in effective and efficient canine signaling: Do pet and working dogs differ?
J. Vet. Behav.
(2018) - et al.
A detailed characterization of loud noise stress: intensity analysis of hypothalamo-pituitary-adrenocortical axis and brain activation
Brain Res.
(2005)
Physiological and behavioral reactivity to stress in thunderstorm-phobic dogs and their caregivers
Appl. Anim. Behav. Sci.
The influence of attention upon anticipatory arousal, habituation and reactivity to a noxious stimulus
J. Res. Personal.
Genetic evaluation of traits in a standardized behavioral test for potential guide dog puppies using crossbreed models
J. Vet. Behav.
Fear of novel and startling stimuli in domestic dogs
Appl. Anim. Behav. Sci.
Assessing fear of novel and startling stimuli in domestic dogs
Appl. Anim. Behav. Sci.
Dogs showing separation-related behaviour exhibit a ‘pessimistic’ cognitive bias
Curr. Biol.
Noise sensitivity, handedness, and the occurrence of high perceived anxiety and depression in young adults
Personality Ind. Diff.
Understanding the genetic basis of canine anxiety: phenotyping dogs for behavioral, neurochemical, and genetic assessment
J. Vet. Behav.
Phenotypic determination of noise reactivity in 3 breeds of working dogs: roles for age, breed and careful assessment
J. Vet. Behav.
Is noise reactivity reflected in auditory response variables including those that measure cognition, in dogs? Initial findings
J. Vet. Behav.
Canine anxieties and phobias: an update on separation anxiety and noise aversions
Vet. Clin. North Am. Small Anim. Pract.
Advances in understanding and treatment of noise phobias
Vet. Clin. North Am. Small Anim. Pract.
Cortisol levels in hair reflect behavioural reactivity of dogs to acoustic stimuli
Res. Vet. Sci.
Noise sensitivity in 17 dog breeds: prevalence, breed risk and correlation with fear in other situations
Appl. Anim. Behav. Sci.
Reliability and validity of a questionnaire survey in canine anxiety research
Appl. Anim. Behav. Sci.
Prevalence, comorbidity and behavioral variation in canine anxiety
J. Vet. Behav.
Behavioral and physiological predictors of guide dog success
J. Vet. Behav.
Associations between motor, sensory and structural lateralisation and guide dog success
Vet. J.
Modular reconfiguration of an auditory control brain network supports adaptive listening behavior
PNAS
Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism
Arch. Gen. Psych.
Genetic analysis of a temperament test as a tool to select against everyday life fearfulness in Rough Collie
J. Anim. Sci.
Stress hormones in the research on cardiovascular effects of noise
Noise Health
Cited by (17)
Rescue dogs show few differences in behavior, cognitive abilities, and personality compared with non-rescue dogs
2023, Journal of Veterinary BehaviorDogs working in schools–Safety awareness and animal welfare
2022, Journal of Veterinary BehaviorCitation Excerpt :At this threshold, humans should wear ear defenders in the workplace, and it has been argued that sensitive canine ears might be damaged as well, possibly even more (Taylor and Mills, 2007; Scheifele et al., 2012). Overall et al. (2019) recommended that dogs should be screened early and repeatedly for their response to various noises. This screening is especially valid for school dogs.
Only when you measure suffering can you fix it
2021, Journal of Veterinary Behavior