ResearchTemperament and lateralization in the domestic dog (Canis familiaris)
Introduction
Lateralization was once thought to be a feature that separated the human brain from the nonhuman animal brain (Berker et al., 1986; Vallortigara, 2006); however, it is now known that lateralization can be observed across a variety of animal species. In the domestic dog (Canis familiaris), for example, evidence suggests that individuals display not only structural lateralization (Tan and Caliskan, 1987a,b; Siniscalchi et al., 2011a; Tomkins et al., 2012) but also behavioral lateralization in the form of paw (see Tomkins et al., 2010a for a review) and movement preferences (Hackert et al., 2008). Such biases have attracted interest in their own right, but are also considered important because they may signify underlying differences in neural functioning. For example, in humans, it is known that movement of a particular limb is associated with an increase in activity in the contralateral cortex that may influence other regions of the same hemisphere (Yousry et al., 1995). In the dog, recent studies have shown that immune responses and catecholamine plasma levels are associated with the paw preference dogs demonstrate on a task requiring the removal of adhesive tape from the nose (Quaranta et al., 2004, 2006, 2008; Siniscalchi et al., 2010a).
Another area that has received some research attention is emotional functioning (Borkenau and Mauer, 2006). Often described in relation to the Valence-Specific (VS) Hypothesis, studies suggest that there may be differences in how the 2 hemispheres of the brain process emotional information (Killgore and Yurgelun-Todd, 2007). Specifically, it has been suggested that the left hemisphere is more strongly involved in the processing of positive approach-related emotions, whereas the right hemisphere is responsible for the processing of negative withdrawal-related emotions (Ahern and Schwartz, 1979; Davidson, 1992). Although it is acknowledged that emotional processing systems are likely to be much more complex and multifaceted than posited by the VS Hypothesis (Killgore and Yurgelun-Todd, 2007), there are nonetheless a number of studies that provide evidence in broad support for some hemispheric differentiation in emotional processing in line with the theory.
The VS Hypothesis has been supported by studies of nonhuman animals. Right-handed primates have been shown to approach and touch more novel objects than their left-handed counterparts (Hopkins and Bennett, 1994; Cameron and Rogers, 1999). Additionally, left-handed adult male macaques are more likely to be socially isolated or attacked by conspecifics, whereas right-handed individuals enjoy more positive interactions with conspecifics (Westergaard et al., 2003). These studies lend support to the VS Hypothesis because they show the left hemisphere to be associated with more positive emotions, such as increased approach behavior in novel contexts and more positive interactions with conspecific animals. They also show the right hemisphere to be associated with negative emotions, characterized by individuals displaying greater latencies to approach and interact with novel objects and experiencing more negative interactions with conspecific animals.
Recent research has reported the relationship between motor laterality and emotional reactivity in the dog. Siniscalchi et al. (2010b) reported that, when simultaneously presented with a dog-shaped silhouette to both the left and right visual fields, dogs displayed no directional bias when turning to view the stimulus. However, when presented with potentially threatening cat- and snake-shaped stimuli, dogs tended to turn their head toward the stimulus located on the left side. Given that the majority of visual input perceived by each eye is processed by the contralateral hemisphere (Cullen et al., 2009), the left directional bias demonstrated by the dogs supports the notion that the right hemisphere is responsible for the expression of fear and aggressive responding (Casperd and Dunbar, 1996). Comparable findings have also been reported in a similar study in which dogs were simultaneously presented with auditory stimuli of differing emotional valence to the left and right sides (Siniscalchi et al., 2008). Even tail-wagging (Quaranta et al., 2007) and nostril usage (Siniscalchi et al., 2011b) in dogs have been demonstrated to be biased and dependent on the emotional valence of the stimuli perceived by the dog.
Behavioral differences have also been reported between individuals with weak and strong lateralization, irrespective of the side that is dominant. For example, dogs demonstrating a stronger strength of paw preference have been found to display reduced latencies to catch a moving object (Batt et al., 2009). Batt et al. (2009) suggested that the willingness of dogs displaying a stronger strength of paw preference to engage with an unfamiliar object indicated that these dogs were bolder in a novel situation. Branson and Rogers (2006) investigated the association between paw preference and noise phobia in a sample of pet dogs and reported that dogs exhibiting a paw preference were less likely than those demonstrating ambilaterality to experience noise phobia. They suggest that lateralization may provide organisms with survival advantages and note that noise phobia is a maladaptive behavioral trait that is likely to be disadvantageous to an individual. Noise phobia has been compared with human anxiety disorders, such as posttraumatic stress disorder, because such conditions also involve the expression of intense negative emotions (Thompson, 1998; Overall, 2000). The human anxiety disorder literature also indicates that people suffering from anxiety disorders and psychosis tend to be weakly lateralized (Chapman and Chapman, 1987; Crow, 1997; Spivak et al., 1998; Parker et al., 1999). Branson and Rogers' (2006) study therefore indicates that the relationship between emotionality and motor laterality may be more complex than the VS Hypothesis suggests.
In this study, we investigated the relationship between motor laterality and temperament in the dog. Temperament is important to dog trainers (Holmes, 1970), dog breeders (Hart and Hart, 1985; Hart, 1995; Podberscek and Serpell, 1996; Segurson et al., 2005), and animal shelter staff. It is a large contributing factor to the surrender of dogs to shelters (Miller et al., 1996; Patronek et al., 1996), and staff also consider temperament in their decision to either adopt out or euthanize surrendered dogs (Vanderborg et al., 1991). Such decisions are highly important for public safety, given the prevalence of dog-bite injuries (Lockwood, 1997; Penny and Reid, 2001; Pillonel, 2001; Uchida et al., 2001). Temperament is also important to humans in that it is one of the primary factors involved in the selection of dogs to perform various service and working roles within the community (Goddard and Beilharz, 1984a,b, 1986; Svartberg, 2002; Svartberg and Forkman, 2002), although it has also been shown that a dog's paw preference can predict its suitability for a working role (Batt et al., 2008a; Tomkins et al., 2012).
Here, we adopted an exploratory approach to further delineate the relationships that exist between laterality and temperament in the dog. Temperament was assessed by administering the Canine Behavioral Assessment and Research Questionnaire (C-BARQ; Hsu and Serpell, 2003) to the owners of pet dogs. The C-BARQ is a comprehensive behavioral assessment that separates temperament traits into 13 subscales, making it an ideal tool with which to probe the nuances of the laterality–temperament interaction. However, we acknowledge that the sensitivity of the C-BARQ to detect differences in behavior that are associated with laterality is not yet known. The various subscales are aggregates of several questionnaire items, a feature that is generally considered to be one of the C-BARQ's strengths, but for the purposes of the current study, may mask subtle effects.
Study hypotheses were based on the principles of the VS Hypothesis, given the extensive body of literature supporting this theory in both human and animal models. It was hypothesized that dogs exhibiting a left paw preference would display higher levels of stranger-directed aggression, stranger-directed fear, dog-directed aggression/fear, attachment/attention seeking, touch sensitivity, owner-directed aggression, and familiar dog aggression. We also hypothesized that there would be differences between lateralized and nonlateralized individuals on some of the C-BARQ subscale items. For example, based on Branson and Rogers' (2006) findings regarding anxiety-related conditions in the dog, it was hypothesized that dogs with a weaker strength of paw preference would exhibit more nonsocial fear and separation-related problems. We also hypothesized that dogs with a weaker strength of paw preference would be more excitable. This was based on Batt et al.'s (2009) report that dogs with a weaker strength of paw preference displayed more excitable behavior when approaching an unfamiliar person than dogs with a stronger strength of paw preference. The strength and direction of paw preference were compared with all temperament items to discover any relationships.
As a final exploratory component, the study also investigated other elements of the dogs and their home environments to identify factors, other than paw preference (e.g., the amount of exercise, training, and grooming the dog received), that may be associated with temperament.
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Subjects
Subjects for the present study were recruited through advertisements placed in local newspapers. The owners of 73 dogs made contact with the experimenter and were provided with detailed information about the study before subsequently agreeing to participate. The sample included 35 male (2 = sexually entire) and 38 female (5 = sexually entire) dogs, aged between 1.25 and 11.50 years (mean = 4.82 years, standard deviation = 3.42). Seventeen dogs were reported by their owners to be crossbred, and
Lateralization in the sample of dogs
According to the z scores, 63.0% of the 73 dogs in the sample demonstrated preferential paw usage and 37.0% did not. When the 3 paw preference groups were compared, 34.2% of dogs demonstrated a left paw preference, 28.8% of dogs exhibited a right paw preference, and the remaining 37.0% exhibited ambilaterality. This distribution did not differ from that which would be expected by chance χ2(2, N = 73) < 1. A binomial test also revealed no significant difference between the numbers of left- and
Discussion
Overall, the study found little evidence in support of a relationship between motor laterality and temperament in domestic dogs. There were no significant differences between the scores obtained by left-pawed, right-pawed, or ambilateral dogs on any of the C-BARQ subscale items. Additionally, there were no statistically significant differences between the scores obtained by lateralized and ambilateral dogs on the C-BARQ items with the exception that on the stranger-directed aggression subscale,
References (71)
- et al.
Differential lateralization for positive versus negative emotion
Neuropsychologia
(1979) - et al.
Factors associated with success in guide dog training
J. Vet. Behav: Clin. Appl. Res.
(2008) - et al.
Two tests for motor laterality in dogs
J. Vet. Behav: Clin. Appl. Res.
(2007) - et al.
The relationships between motor lateralization, salivary cortisol concentrations and behavior in dogs
J. Vet. Behav: Clin. Appl. Res.
(2009) - et al.
Owner-companion dog interactions: relationships between demographic variables, potentially problematic behaviors, training engagement and shared activities
Appl. Anim. Behav. Sci.
(2007) - et al.
Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons
Behav. Processes
(1996) Anterior cerebral asymmetry and the nature of emotion
Brain Cogn.
(1992)- et al.
External factors and reproducibility of the behaviour test in German shepherd dogs in Switzerland
Appl. Anim. Behav. Sci.
(2005) - et al.
Handling in infancy, brain laterality and muricide in rats
Behav. Brain Res.
(1983) - et al.
A factor-analysis of fearfulness in potential guide dogs
Appl. Anim. Behav. Sci.
(1984)