ResearchLateralization in the domestic dog (Canis familiaris): Relationships between structural, motor, and sensory laterality
Introduction
Hemispheric lateralization refers to the specialized functions of the left and right sides of the brain, which result in observable differences in the use of the left and right sides of the body for both motor and sensory tasks (Vallortigara et al., 1998). Lateralization is no longer thought to be unique to humans, but instead is considered a characteristic of most vertebrates (Rogers and Andrew, 2002), with the right hemisphere primarily controlling rapid responses, while the left controls considered responses (Rogers, 2002). Possessing a lateralized brain offers several advantages at both the individual and population level, and in particular, in nondomesticated animals. At the individual level, enhanced performance and faster responses are seen in lateralized compared with nonlateralized subjects, regardless of the direction of laterality (Rogers, 2002). At the population level, the extent to which a group is lateralized in the same direction can assist with survival because of both intraspecific social behavior and avoidance of predation (Rogers, 2000).
The extent to which lateralization influences the lives of companion animals is continuing to be explored. Dogs play an important role in society, both as companions and as workers. By convention, service dogs such as guide dogs are left-heel trained, and as such are required to work on the left side of their handler. This convention may prove to be a disadvantage to dogs that are less flexible when turning right, and may result in their being disqualified erroneously from training. Potentially, less flexible right-turning dogs may turn out to be just as suitable for guiding work if trained on the right side of their handler.
Visual biases may also influence suitability of dogs for work if they are particularly reliant on their right field of vision and corresponding brain hemisphere, which is often obscured by the handler when undertaking left-heel work. This bias has been reported in guide dogs where left visually preferent dogs were more successful in the Guide Dog Training Program than right visually preferent animals (Tomkins et al., 2011).
In comparison with motor and sensory lateralization, structural lateralization has received very little scientific attention. Structural asymmetries are evident in the positioning of some internal organs, such as the heart. Hair whorls, anatomical features of the hair coat that can show left-right asymmetry, are also of interest as a structural marker of lateralization (Jansen et al., 2007, Tomkins and McGreevy, 2010a, Tomkins and McGreevy, 2010b) since the nervous system and the integument have common origins in the structure of the embryo (Smith and Gong, 1973). Given that whorls are not influenced by maturation or human intervention, they could potentially provide an external indicator of functional brain lateralization. In addition, some whorl characteristics (presence and direction) are binary outcomes, unlike motor and sensory measures that can result in animals being classified as right preferent, left preferent, or ambidextrous; thus, hair whorls may offer a more compelling tool for determining lateralization in animals.
Given that significant resources are involved in training service dogs such as police and guide dogs, determining early predictors of success is attractive to industry stakeholders. Measures of laterality, such as hair whorls, may reliably indicate suitability among dogs intended for work. An association between hair whorl characteristics and behavioral tendencies in the dog has been reported (Tomkins and McGreevy, 2010a, Tomkins et al., 2011), which has largely been focused on the chest whorl. In our preliminary study assessing hair whorl characteristics in dogs (n = 120) of various breeds and cross-breeds, the source of the dog (shelter or nonshelter) was marginally associated with the position of the chest whorl (Tomkins and McGreevy, 2010a). Dogs sourced from a shelter had a tendency for their chest whorls to be positioned further away from the thoracic inlet than nonshelter dogs. Given behavioral reasons are known to be the leading cause of relinquishment of dogs to shelters (Salman et al., 2000), it seems plausible that an association between chest whorl position and behavior exists. Furthermore, hair whorls were assessed in potential guide dogs (n = 114), and the direction of a chest whorl was found to be significantly associated with the success of a dog in the Guide Dog Training Program, where dogs with a counter-clockwise (CC) chest whorl had a higher probability of success than dogs with a clockwise (C) whorl (Tomkins et al., 2011).
Very few animal studies have compared hair whorls with other laterality measures such as motor lateralization. Murphy and Arkins, 2004, Murphy and Arkins, 2005, Murphy and Arkins, 2008 investigated the relationship between cephalic hair whorls and motor laterality in the horse. The authors reported that foals with C whorls presented their right foreleg initially at birth (Murphy and Arkins, 2005); and, that, left-lateralized horses exhibited significantly more CC whorls, whereas right-lateralized horses had more C whorls than expected by chance (Murphy and Arkins, 2004, Murphy and Arkins, 2008). Although a significant relationship was reported by Murphy and Arkins, to the best of our knowledge, no studies have made a comparison between noncephalic hair whorls and measures of laterality. Furthermore, only limited literature is available on canine hair whorl characteristics (Tomkins and McGreevy, 2010a, Tomkins and McGreevy, 2010b, Tomkins et al., 2011).
Studies have demonstrated that hair whorl characteristics are associated with behavioral tendencies (cattle: Grandin et al., 1995, Randle, 1998, Lanier et al., 2001; horses: Górecka et al., 2006; dogs: Tomkins and McGreevy, 2010a, Tomkins et al., 2011). A review of the literature revealed that there is a dearth of comparable data on different measures of lateralization, especially those reflecting structural lateralization. Therefore, the primary aim of this study was to compare this measure of structural lateralization with both motor and sensory laterality measures. In addition, the relationship between motor and sensory lateralization was assessed. For our study these comparisons were made in dogs, a species in which hair whorls (at 11 different regions) have been reported as a structural marker of lateralization, motor lateralization can be determined using 2 different tests (Kong and First-stepping Tests), and sensory lateralization in the form of visual bias can be determined using the Sensory Jump Test (5 measures used). The presence and direction of hair whorls were assessed for structural lateralization, while direction and strength of lateralization were measured for both motor and sensory lateralization. Direction of lateralization indicates the direction of bias (either left or right preference), whereas strength of lateralization captures asymmetry in the activity of the 2 appendages (paws for motor laterality) or organs (eyes for sensory laterality), without taking into account the direction of the preference.
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Animals
Dogs participating in the laterality study were aged between 13 and 17 months, and sourced from Guide Dogs NSW/ACT. The cohort of trainee guide dogs (n = 114) were all neutered (males, n = 53; females, n = 61), and included Labrador retrievers (n = 97), golden retrievers (n = 9), and Labrador–golden retriever crosses (n = 8). Although the full cohort (n = 114) of dogs participated in the Kong Test (motor lateralization) and hair whorl assessments, only a portion of these dogs were assessed in
Hair whorl characteristics
The presence, direction, and classification of whorls that are located bilaterally or centrally can be seen in Table 1, Table 2, respectively. Briefly, in more than 10% of the dogs, whorls were present in the ventral mandibular, chest, brachial and thoracic axillary, elbow, and ischiatic regions. Whorls were uniformly classified as simple, with the exception of those on the elbows and chest, which were consistently tufted. Because of the lack of variation in simple and tufted whorl
Discussion
To our knowledge, this is the first study to report on the relationship between the 3 measures of laterality, that is, structural, motor, and sensory. Several associations were identified between structural and motor, structural and sensory, and motor and sensory lateralization.
The findings of our study support the association between structural and motor laterality measures in the horse reported by Murphy and Arkins, 2004, Murphy and Arkins, 2008. Similar to the studies performed by Murphy and
Conclusion
To our knowledge, this is one of the first studies to assess all 3 measures of laterality (structural, motor, and sensory lateralization), and furthermore, the first to assess the relationship between these measures. The presence and direction of whorls in several regions were associated with motor and sensory measures. Given measures of laterality have been associated with identifying dogs suitable for working environments, morphological indictors of laterality such as hair whorls may provide
Acknowledgments
The authors thank Guide Dogs NSW/ACT for providing the facility and dogs to conduct this study. The Australian Research Council and Guide Dogs NSW/ACT provided funding for this project. The authors also thank the 2 anonymous referees whose comments on this article were greatly valued.
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None of the authors of this article have a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the article.