Overview

Noise reactivity is a common problem for dogs and may progress to true phobia (Overall et al. 2001; Sherman, Mills 2008; Dale et al. 2011; Blackwell et al. 2013; Overall 2013). Such reactivity can severely compromise function in both pet and working dogs. Noise reactivity may be comorbid with many canine (Overall et al. 2001) and human anxiety disorders and is thought to be important in human conditions where information processing is affected. We are evaluating whether the same patterns pertain in dogs as part of an ongoing study on canine cognition, anxiety and performance.

Introduction

Diagnoses in veterinary behavioral medicine act as functional, phenotypic, phenomenological rules for grouping patients with certain behaviors and/or signs of behavioral problems with those who most like them, while distinguishing dogs who are 'different' based on patterns of behaviors, behavioral responses and behavioral response surfaces. In other words, dogs who are anxious when exposed to noise, may not be anxious when left alone, and the rule for separating dogs in those 2 groups of concern depends in part on which stimulus provokes the distress. These diagnostic rules or definitional criteria function to cluster groups of behavioral responses or response surfaces that may share in common some underlying mechanisms of action, and, as a result, clusters of more targeted treatments.

The first step in any behavioral evaluation is to ask where in the distribution of canine behaviors - normal and abnormal - any dog fits (see Figure 1). The problem encountered in any field, but which is especially painful in veterinary behavior, is that we may not know the range of species- or breed-associated behaviors, given the number of situations in which dogs live.

Figure 1 Schematic for a way of thinking about the universe or set of canine behaviors and whether they are normal for the species and breed, beginning to deviate from normal or abnormal, regardless of the underlying pathology and mechanisms driving it (Adapted from: Overall, 2013).

Additionally, behaviors noted as 'normal,' 'perfect,' 'problematic,' et cetera may neither be noticed nor reported in frequencies that reflect occurrence (Figure 2).

Figure 2 Clients can like problematic or abnormal behaviors and not like normal ones, and how clients feel about, perceive, notice and understand canine behaviors affects which behaviors scientists and clinicians get to witness and test. No assumptions about the normality or the distribution of behaviors should be made on the sole basis of such reports (Adapted from: Overall, 2013).

Finally, we usually lack criteria to cluster dogs in more vs. less similar groups and almost always lack objective tests that would confirm such groupings. This is a common problem in understanding patterns of appearance and behavior and is well illustrated using bird species. Birds look different and most of us could cluster them in same or different piles, but there is a lot of variation that goes with the environment. If you also use bird song, you have another measure by which you can sort them into more vs. less similar, and if you add genetic analysis, even unresolved birds will cluster by species, and all 3 measures will be concordant. Needless to say, good bird watchers will do a better job of sorting all the species by looks or vocal repertoire than will poor birdwatchers...a pattern we should also expect for dogs.

Defining Noise Reactions

Objective testing is especially important in behavior and behavioral medicine because the dog's behavior is the final common integrative pathway of all of the organ system and molecular responses, and it may be relatively nonspecific, compared to the pattern/clustering of the mechanisms driving it. Noise and storm phobias are fairly clear, but, as they are developing, clients often worry about the dog's ability to see or hear well, and about whether physical pain is driving the behavior. Accordingly, any time any suite of behaviors is evaluated for normality, the whole dog should be evaluated. In the case of behavioral concerns, it is important to rule out somatic or other cognitive/mental/behavioral conditions that may be misleading. Pain, poor hearing and poor vision all may contribute to altered reactivity to noise. Extremely acute hearing is difficult but not impossible to evaluate clinically, but the behavioral pattern should distinguish between a phobic response and a dog who has enhanced auditory skills. Early in the development of these conditions, clients may recognize extreme fear but may not correctly identify the stimulus, so the dog should be screened for all potential fears.

For the purposes of this set of studies, we define canine noise responses as follow (Overall 2013).

 Diagnostic criteria and description for noise phobia

 Profound, non-graded, extreme response to noise manifest as intense avoidance, escape, or anxiety and associated with the sympathetic branch of the ANS.

 Diagnostic criteria and description for storm phobia

 Profound, non-graded, extreme response to some aspect of the storm (accompanying noise, wind, lightening, wind, thunder, ozone levels, changes in barometric pressure, alterations in illumination, et cetera) manifest as intense avoidance, escape, or anxiety and associated with the sympathetic branch of the ANS.

 Diagnostic criteria and description for noise/storm phobia

 The behaviors can include mania or catatonia, concomitant with decreased sensitivity to pain or social stimuli.

 Once established repeated exposure results in an invariant pattern of response.

These subtly varying definitions are not meant to imply that these conditions are completely separate. They may vary in important mechanistic ways that we will fail to understand if we lump everything into one diagnostic category. What those who are fond of terminological simplicity often fail to realize that if you split categories, you can later test mathematically for similarity and combine them. If you lump everything at the outside, you cannot recover differences. Noise and storm phobia may have overlapping pathologies, overlapping risk factors, and overlapping phenotypes, but they are not the same because many more stimuli are involved in storms than in most noises. Our data suggest that the noise responses can be complex, and responses of dogs to various noises can be complex.

 The response of dogs to storms and gunshots appears to be similar.

 The response of dogs to fireworks is different from their response to storms and gunshots, possibly because of the extreme visual component to the stimulus.

 From the data collected on comorbidity, we know that reactivity/phobia to general noises appears to be a different condition from reactivity/phobia to noises associated with storms.

 The extent to which these differences may matter for treatment is unclear, but they become important for phenotypic and genetic studies of reactivity/phobia in dogs.

Dogs who are continuously and characteristically distressed when exposed to noises/storms but who do not meet the criteria for a 'phobia' may best be classified as 'reactive' and monitored, treating as warranted by signs. We need to consider that predictability of the triggering stimulus, or lack thereof, may be responsible for the dog's reaction, and that the dog's reaction is not independent of training, exposure, learning and conditioning (Dale et al. 2010; Overall 2013). The distinction between 'reactivity' and 'phobia' remains blurry. Well-controlled dogs can look 'reactive.' We do not know if all 'reactive' dogs will go on to be 'phobic,' given time and exposure. Logic argues that dogs who respond with concern to noise but lack the complete 'phobic' criteria should be labeled as 'reactive' and closely monitored.

Common nonspecific signs associated with noise reactivity/phobia may also be shared by other anxiety-related conditions (Mariti et al. 2011; Overall 2013):

 Urination

 Defecation

 Salivation destruction

 Panting

 Pacing

 Freezing/immobility trembling/shaking

 Vocalization (bark, whine, growl, howl)

 Escape behaviors

 Vomiting

 Diarrhea

 Mydriasis*
*Clients are able to recognize mydriasis more easily in situations of noise phobia than they can for many other phobias or panicky situations and so it may be a useful sign to monitor.

Some dogs may show suites of correlated behaviors. For example, salivation appears to occur more commonly in dogs who freeze and become immobile. Clients will wish to note which suites of behaviors their dogs exhibit so that they can monitor these nonspecific signs for changes (hopefully, improvement) during treatment.

Comorbidity

There is evidence that if dogs react to or are phobic of noises in a repeatable manner, they may have an increased incidence of separation anxiety and/or other anxiety-related conditions (Overall et al. 2001; Blackwell et al. 2013). It is critical to screen for comorbid conditions because unless all aspects of the dog's distress are treated, the dog will not improve (Overall et al. 2014). The most common and profoundly debilitating comorbid conditions include panic disorder (PD) and noise and storm phobias. In one study of 141 dogs who met the diagnostic criteria for separation anxiety, noise phobia, or both during the course of a year in which all behavior clinic patients were screened using the same instrument, comorbidity was significantly greater than would be expected by chance alone (Overall et al. 2001). This suggests that being affected by one condition may predispose one, likely at the neurochemical level, to be affected by another.

The 'risks' of comorbidity in this population, based on the estimated conditional probabilities, were as follow (Overall et al. 2001) (SA = separation anxiety; TP = storm phobia; NP = noise phobia)

 P [SA/TP] = 0.8701 (87%)

 P [TP/SA] = 0.6147 (61%)

The probability that the dog had separation anxiety given that he had storm phobia here was 0.87 or 87%. The probability of the reverse - that the dog had storm phobia given that he had separation anxiety - was only 0.61 or 61%. That these are not identical suggests that these are different conditions.

 P [SA/NP] = 0.8804 (88%)

 P [NP/SA] = 0.7364 (74%)

The probability that the dog had separation anxiety given that he had noise phobia - which was defined here as any non-storm noise - was virtually the same as for storm phobia, 0.88 (88%). The probability that a dog with separation anxiety had noise phobia - a more generalized response - was greater than for storm phobia, 0.74 or 74%.

 P [TP/NP] = 0.7609 (76%)

 P [NP/TP] = 0.8974 (90%)

For noise and storm phobia, the probability that you have one, given that you have the other, is not equal, suggesting that these are 2 different reactions in dogs. The chance of having a noise phobia, given that you have a storm phobia, was 0.89 or 90% suggesting that the unpredictable nature of storms may play some role in how reactive dogs become across all noises.

These data argue convincingly that in terms of comorbidity of separation anxiety, noises associated with storms and those associated with all other stimuli, combined, are similar, but the comorbidity of noise reactions, themselves, suggests underlying mechanistic variation. This is a non-trivial finding when we consider the effects of cognition.

Comparisons of Herding Dog Reactivity Scores

To better evaluate dogs with anxiety-related conditions we hypothesize affect each other's mechanisms, we created a scoring system of behavioral responses that clients can observe and report derived from the separation anxiety and noise phobia/reactivity screen (SANP) (Overall et al. 2006; Overall 2013). This system provides an anxiety intensity rank (AIR score) that allows us to compare dogs (i.e., within vs. between litters, within vs. across breeds/lines, et cetera) and compare behaviors over time (i.e., with age, with treatment), without losing the valuable phenotypic information that may be important for us to identify underlying molecular and regional brain regions responsible for worrisome responses. Instructions for how to calculate these scores, and an example, are found in Box 1.

We used these tools to evaluate behavioral and demographic information collected for 165 Australian shepherds (AUS), 211 Border collies (BOC), and 93 German shepherds (GSD). Behaviors were compared using a metric that includes type, frequency, and intensity of response and AIR score. Reactivity to noise segregates in family lines, although individuals within families may have considerable variation in noise response. Such variation may be time and exposure dependent, which can present a phenotyping challenge.

The mean AIR scores for Australian shepherds and Border collies are not significantly different, but both differ significantly from those of German shepherds, which are considerably lower. In the dogs studied here, GSD are less affected by noise reactivity than are AUS and BOC (AUS x BOC, ns, p = 0.322; F-test; AUS x GSD & BOC x GSD, p = 0.00001; F-test).

The presence and intensity of reactivity varied with age, and this pattern differed across breeds. In this study, Border collies are older than Australian shepherds and both are older than German shepherds, but the distribution of ages suggests that young and immature dogs were not part of the study population. Border collies and Australian shepherds were more severely affected than were German shepherds. Source/purpose of dog may also affect severity of affliction. Age matters when assessing these phenotypes, and these data imply that accurate dichotomous phenotypic assessment is possible at a relatively early age, providing for both humane treatment and accurate phenotyping that facilitates good genotyping. In German shepherds in this study, older dogs had lower scores than younger dogs. It is important to remember that these data are a snapshot in time. No dogs were followed through time, so no time-penetrant patterns should be assumed.

The reactions exhibited by these 3 breeds were not simply general noise responses, but responses to specific stimuli. Border collies and Australian shepherds exhibited one set of behaviors when distressed, German shepherds exhibited another. One can conclude that although they all met the diagnostic criteria listed, their morphs of response - or phenotypes - were not the same. Certainly, the brain regions involved in such different responses differ. In all cases, reactions to different stimuli were highly comorbid. Whether this comorbidity is due to shared neurochemical mechanisms or changes in underlying neurochemical substrate caused by 1 stimulus is not known. For owners treating these dogs, knowledge of such comorbid conditions is essential if treatment is to be successful.

Early data indicate that dogs who are calmer, solve cognitive tests better, more efficiently, with fewer errors and in less time than do reactive dogs. Dogs who react to noises are not as efficient at cognitive tasks, even if they do not completely shut down. The logical sequela to these findings is that heightened reactivity interferes with cognitive behaviors, likely including those related to social interactions, which require subtle shifts in response on a context-by-context basis. Reactivity then becomes both a behavioral and welfare issue for dogs, regardless of whether someone thinks that the dog is 'coping' just fine. We should consider that measurement of behaviors in contexts that are meaningful to the dog could be enlightening.

Box 1. Quantifying changes in behavior for dogs treated for noise reactivity and/or separation anxiety - AIR and SAIR scores (from Overall 2013)

Using intensity, severity and reactivity scores, we create an 'anxiety score.' For the purposes of the separation anxiety and noise phobia/reactivity screen (SANP) we can calculate separate separation anxiety and noise reactivity scores. For noise reactivity, we have created an anxiety intensity rank (AIR score) that allows us to compare reactive dogs and to compare individual dogs before and after treatment.

The AIR score is calculated as follows:

Step 1: Note the situations in which a distressed response of any kind is seen and assign a score based on frequency of response.

1.  Storms/thunderstorms

2.  Gunshots

3.  Fireworks

4.  Other noises

For each of these situations assign a score that correlates with the frequency with which the dog reacts, once exposed in a way that matches the terminology used in the SANP section of the questionnaire, as follows (Table A).

Table A. Frequency category of the dog's reaction to any noise, once he encounters it, and the score assigned to that category of frequency

Step 2: Count the number of behavioral responses the dog exhibits when exposed to the situations. For noise reactions, there are 11 possible behaviors exhibited, not all of which are equally easy for clients to see, but when comparing dogs before and after treatment we can assume that clients will see the same behaviors for comparison. The 11 listed behaviors are salivate, hide, defecate, tremble, urinate, destroy, escape, freeze, pant, will not eat food/treats, pace, pupil dilation, and vocalize (bark, whine, growl, howl). Clients are welcome to include a category of 'other,' if they wish.

Step 3: Multiply the number of signs by the frequency score for each trigger of the reactions, then sum these to provide the AIR score.

To see the utility in this approach, we can compare 2 dogs, both border collies. Table B shows the score calculations for border collie 1, and Table C shows the score calculations for border collie 2.

Table B. AIR score calculation for a very noise reactive dog

Table C. AIR score calculation for a dog who is really not noise reactive at all

Clients who have noise reactive/phobic dogs can recalculate the AIR score at set times during treatment to obtain some more objective measurement of behavioral change and so determine which situations may need more help.

Because reactions to noise and absence can be manifest as comorbid conditions, a similar approach can be taken for dogs who are left when distressed. In the SANP section of the questionnaire we ask about the following behaviors when left for real and in a 'virtual' absence:

 Destructive behavior when separated from the client(s)

 Urination when separated from client(s)

 Defecation when separated from client(s)

 Vocalization when separated from client(s)

 Salivation when separated from client(s)

 Panting when separated from client(s)

We use the same frequency categories that we did for noise reactivity and phobia. So a separation anxiety intensity rank (SAIR) score can be calculated as shown in the following example (Table D).

Table D. SAIR rank calculations for a dog

SAIR rank calculations for a dog who destroys every time he is really left, vocalizes 40–60% of the time he is really left and salivates less than 40% of the time he is really left (3 signs, total: 1 sign at a score of 4, 1 sign at a score of 1.5 and 1 sign at a score of 1). When his virtual absences are assessed, he destroys and vocalizes less than 40% of the time when he does not have access to his people for 2 scores of 1.

This type of calculation will help provide both the clinician and client with some more objective assessment of improvements or relapses that the dog is experiencing during treatment, and will also help clients to monitor dogs who are genetic risk as they mature.

Acknowledgments

Funding for earlier and ongoing reactivity studies and canine cognitive tests has been provided by DARPA (Defense Advanced Research Projects Agency) grant 52731-LS-DRP, and DARPA/UES grant P845, ARO grant W911NF-07-1-0074/52731 to KLO, ARO/DARPA grant W911NF-14-1-0574 to AED & KLO. Sincere thanks to Soraya Juarbe-Diaz, DVB, DACVB for technical help and for refining the construction of the AIR/SAIR score.

References

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