Author Names: Charlotte Handley (BSc (Hons) Bioveterinary Science) and Dr Alison Wills
Existing canine research aims to investigate laterality in relation to many aspects of behaviour, ranging from sniffing with a preferred nostril, to tail wagging. Currently, there is a lack of research focusing on laterality and asymmetry in conditioning. This information could prove beneficial, enabling adaptation of training protocols or increasing safety for racing animals, their riders and handlers. Healthy, mixed breed dogs (n=19) of mean age 4.9±3.16 years were chosen. Dogs were of mixed sex (7 male, 12 female) and mixed reproductive status (7 intact, 12 neutered). First Step testing was carried out to determine strength of laterality. The z-score was calculated to establish a cut off for ambidexterity. Muscle measurements were taken, by spring tension tape measure, for each leg and the difference between sides was calculated. The z-score identified 10 animals to be ambidextrous, 6 to be left pawed and 3 right, a contrasting spread of results to that reported in the literature. A significant relationship was found between strength of laterality and difference in muscle mass in the hindlimbs (P<0.020). No relationship was seen between strength of laterality and muscle mass in the forelimbs (P=0.927). A significant relationship was also found between age and difference in hindlimb muscle mass (P<0.005). Further standardised research would be beneficial in this area. Particular emphasis on single breed selection, or the utilisation of a larger sample of mixed breeds, would increase the external validity of the study. Confounding factors, including unilateral gait issues, were controlled for, but future access to veterinary records may allow a more informed judgement for inclusion and exclusion criteria.
Human interest in the laterality of animals has seen many species extensively studied, including dogs (Batt et al., 2007), horses (McGreevy and Rogers, 2004), primates (Pouydebat et al., 2014) and mice (Ribeiro-Carvalho et al., (2010) among others. Strokens, Gunturkun and Ocklenburg (2013) carried out a laterality assessment of 116 animal species including various amphibians, reptiles and birds. Despite this, to the researchers’ knowledge, laterality and muscle mass have never been studied together in the domestic dog (Canis familiaris).
1.1 Human research
Many human studies have used limb measurements as a tool for volumetric assessment. Mohan et al., (2014) and Li et al., (2010) studied the relationship between maximal hand grip strength and difference in limb circumference in adults. Both authors found a greater circumference in the wrist, fore and upper arm of the limb deemed to be ‘dominant’. Dylke et al., (2012) note that circumference measurements are considered the gold standard for volumetric measurement of limbs in cases of lymphoedema, requiring frequent monitoring. This study also agrees with MacDonald, Allen and Monteith, (2013) who state a direct link between muscle mass and limb circumference.
1.2 Equine laterality
Laterality in horses has been extensively studied owing to its importance in riding performance. Symes and Ellis (2009) report equine asymmetry to be a contributing factor to rider asymmetry and conversely, that the rider can compound unevenness in the horse. Warren-Smith and McGreevy (2010) report the ability of asymmetry to influence horse stability and it is noted by Wells and Blanche (2007) that horses may be thrown off balance in severe cases. This is especially the case when cornering with rider and Tan and Wilson (2009) discuss the observed increase in effective body weight. The authors studied cornering in field conditions (n=16) and recorded an increase in gravity and acceleration during the turn, exacerbated by the mass of the rider. Pfau et al., (2009) discuss the increased metabolic cost associated with carrying a rider, noting that cost is reduced with shortened stirrups, a well-positioned saddle and an experienced rider. The horse must support the weight of the rider but does not have to move them through each stride, due to the elastic coupling of load bearer and rider. Kang et al., (2010) state that if the rider has incorrect body or saddle position this can result in increased asymmetry in balance. Peham et al., (2004) also discusses saddle position and fit, finding motion patterns disturbed by poor position and mounting. Thompson, McGreevy and McManus (2015) discuss increased rearing and bucking behaviour when riders have poor stability and balance. The authors attribute this to saddles and equipment, which if poorly fitted, cause miscommunication between rider and horse leading to difficulty handling and safety concerns.
Dressage and show jumping performance can also be negatively affected by asymmetry (Luicidi et al., 2012). It was observed by Murphy, Sutherland and Arkins (2005) that riders will often halt horses approaching a jump to readjust stride pattern, allowing the horse to jump on the preferred lead. van Heel et al., (2010) also observed preference affecting show jumping due to unevenness in hooves, created by uneven wear and tear.
McGreevy and Rogers (2004) documented the direction of galloping on race-tracks (national and international) to vary, depending on location. Knowledge of individual laterality may have the ability to allow selection of horses for racing based on a favourable limb or side, aiding cornering balance and horse and rider safety as discussed by Alexander (2002). The paper evaluates the vertebrate gait, using horse barrel racing as an example. The author discusses horses leaning in to a corner to reduce the risk of rolling over. In cases of asymmetry this may cause over, or under balance, although studies in this field are currently lacking.
Limb preference and balance may also have an impact on hoof grip when contacting softer ground. Harvey, Williams and Singer (2012) studied the use of hoof studs during competition on turf. Studs were most efficacious in reducing cranio-caudal foot slip during cantering, when used on the trailing limb rather than leading limb, giving additional grip to the hoof positioned more caudally under the body. These findings have wider implications, Hitchens et al., (2010) found higher incidence of injury on turf than sand or dirt. Use of studs in the non-preferred limb may improve horse and rider safety and stability on turf, this would appear to warrant further investigation.
Murphy and Arkins (2008) state that uneven conditioning in horses is avoidable if owners and trainers exercise animals evenly. Oosterlinck et al., (2013) and Siniscalchi et al., (2014) speculate that one-sided handling of horses is likely to contribute to asymmetry. The authors note greater symmetry in unridden horses than those frequently handled and ridden, although conversely it was observed by McGreevy and Rogers (2004), that Standardbreds, yet to be broken in, also demonstrated limited lateralisation. It is of note that the sample were only 8 months old, asymmetry may not have manifested by that age. However, van Heel et al., (2010), in a study aimed to predict future laterality, looked at youngsters displaying subtle hoof placement preference. A strong correlation was found between preference at foal and retest as adult. The sample size for retest was very small though (n=4), due to movement of horses, so it is difficult to generalise these findings to the equine population.
Knowledge of equine laterality is beneficial to be able to counter balance issues that may pose a safety concern for riders (Murphy, Sutherland and Arkins, 2005). It would seem appropriate that this principle would apply to dogs, especially those used in sporting activities, although this has not been studied to date.
1.3 Canine laterality
Different laterality behaviours have been investigated and laterality has been established in tail wagging (Siniscalchi et al., 2013; Quaranta, Siniscalchi and Vallortigara, 2007), sensory, olfactory and visual behaviour (Siniscalchi et al., 2011; Tomkins et al., 2010) and also motor preference (Marshall-Pescini et al., 2013). There have been studies into relationships between laterality and noise phobia in guide dog training, enabling selection of less nervous and noise phobic dogs to fulfil their daily tasks (Schneider, Delfabbro and Burns, 2013; Batt et al., 2008; Branson and Rogers, 2006).
In the first canine laterality study by Tan (1987), motor laterality was assessed by removal of a plaster from the eyes. Use of each paw was recorded until the sum of right and left reached 100. 57.1% of dogs (n=28) were right-pawed, 17.9% left and 25.0% ambidextrous. In later research, this method was superseded by those deemed to be ‘better’, including the ‘First Step’ test piloted by Tomkins, Thomson and McGreevy (2010). First Step was deemed to be preferable due to the lack of training influence and practice.
Wells (2003), (n=53), used three manual tasks to compare paw preferences (giving paw, removing blanket from head, retrieving food from can). Dogs were shown to have stronger preferences in the ‘give paw’ task. Both Wells (2003) and Poyser, Caldwell and Cobb (2006) evaluated ‘Give Paw’, stating that it may present learned behaviours, rather than true lateralisation. Ribeiro, Eales and Biddle (2011) studied this learning concept in mice, recording a positive correlation between previous successful paw choices in gaining food (retrieval from a tube) and future paw choice, indicating that in that species, a degree of learning can influence later choices. It is important to consider tests which do not see training influence, hence the use of First Step in the present study.
Hackert et al., (2008) studied galloping actions and paw preference in dogs. They ascertained the leading forelimb in quadrupeds to be that which lands furthest forward in the stride, agreeing with Fischer (2011) who studied canine movement in relation to breed. It is commented by Schmidt (2011) and Biewener (2003), that this limb is usually second to contact the ground in quadrupedal mammals. In the study by Hackert et al., (2008) there is noted to be a limited sample size (n=5), the authors discuss the need for further canine research to generalise these findings.
Research by Lee, Konno and Hasegawa (2011) found left pawed dogs to be less sociable and more neurotic. Interestingly in comparison with equine literature, left-footed horses were found by Murphy and Arkins (2008) to be more volatile, requiring more discipline. This may suggest a left sided trait for behavioural issues, warranting further investigation. However, there are methodological issues with the Lee, Konno and Hasegawa (2011) study. Owner questionnaires were used to ascertain levels of aggression, neuroticism, and sociability (among other parameters). Owners may have been more generous due to subjectivity and not wishing to have their dog labelled as ‘aggressive’. It was noted by Temesi, Turcsan and Miklosi (2014) that lack of standardisation in owner questionnaires concerning negative behaviours has a great impact on results, with inability to generalise between studies due to this lack of standardisation. The authors do note, however, that strong correlations were seen between owner judgements and independent subject behaviour ratings.
In dogs, bodyweight is distributed unevenly through the limbs. Thoracic limbs support approximately 60% and pelvic limbs 40% of mass (Goldner et al., 2015). Power generation for locomotion is powered by the hind limbs, through torque about the hip and extension of the back (Usherwood and Wilson, 2005). This is in contrast to human bipedal locomotion, which is powered by limb muscle extension (Williams et al., 2009). Dogs conditioned for endurance pulling can be seen to grip the ground and drag forwards using both their core muscles and forelimbs (figure 1).
Figure 1. Image showing weight pull using the forelimbs (BullyMax®, 2015).
This forwards pulling is also the case, to a lesser degree, in dogs pulling on the lead. Ogburn et al., (1998) discussed increased pressure through the front of the neck when dogs pull on traditional neck collars. Less pulling behaviour was observed in subjects when a head harness was used designed to put pressure through the back of the head, into the scruff. Pressure distribution away from the trachea can also reduce the incidence of tracheal collapse in susceptible individuals, as recorded by Maggoire (2014), who noted certain size predisposition in miniature and toy breed dogs. Pauli et al., (2006) observed greatly increased intraocular pressures in dogs walked on the lead compared to a harness, due to compression of the jugular vein by the lead tension. Other injuries can also occur through excessive pulling on the neck and forequarters. Hallgren, (1992) found that 63% of studied dogs (n=400) had neck or spinal injuries, of those, 91% were reported to have experienced jerking or had pulled on the lead during walks. This poses a health risk to animals that relentlessly pull forwards through the neck and spine.
Weight pulling for sport has been the subject of little study. Pasi and Carrier (2003) note, in these endurance breeds (generally brachiocephalic bull type), there is a trade-off between speed and strength in conformation. The authors note that this may not naturally be the case, rather a result of long-term human manipulation of breeding lines, also speculated by Lark, Chase and Sutter (2006).
In cases of assistance dogs, there has been a movement towards use of harnesses, especially for guide dogs and those pulling wheelchairs (Peham et al., 2013). The force required to pull wheelchairs (approximately 29.3N (Coppinger, Coppinger and Skillings 1998) was investigated by Peham et al. (2013). Forces through different harnesses when dogs were working (up to 8 hours/day) were investigated. Most force was exerted under the trunk and sternum, shunting weight from the harness and hind through the forelimbs. Force was found to decrease with use of harnesses that were both padded and gave support along the spine, reducing abnormal loading of the forelimbs, seeing more symmetrical conditioning. There is little current study of the effects of leads and harness with regard to weight shifting in dogs, an area where further study may be beneficial.
1.3.2 Racing Greyhounds
Greyhounds have been bred for speed, with the ability to reach 19m/s on the racetrack, with increased aerobic capacity over similarly built breeds (Hudson et al., 2009). Research by Sicard, Short and Manley (1999), note that most greyhound injuries occur in the first turn of a race, when participant density is greatest and greyhounds are migrating to take the favoured route. It is noted that in track greyhounds, racing is in an anticlockwise direction, with the majority (96%) of metatarsal injuries acquired on the right side (Payne, 2013; Johnson, Skinner and Muir, 2001). Piras and Johnson (2006) comment that this is due to the right hind giving propulsion while counteracting centrifugal forces. The central tarsal bone is subject to intense compression forces while navigating a curved track, leading to failure and fracture. Usherwood and Wilson (2005) observed that Greyhounds do not slow down nor change foot contact timing to counter this force when cornering. This was noted to result in an increased limb force of 65%, however, track banking was not disclosed, which may have altered observed forces. Banking has been investigated in humans by Damavandi, Dixon and Pearsall (2012), with greatest force changes seen mediolaterally (530% increase at 10º compared to flat). The authors discuss the substantial asymmetric adaptation of ground reaction force (GRF), discussing muscular and postural adaptations necessary to enhance dynamic stability. This is in contrast to equine banking research by Hobbs, Licka and Polman (2011) studying increases in centripetal force. They noted that greater body tilt was created on a flat curve than banked curve at walk (5.3º versus -2.1º), trot (18.8º versus 9.5º) and canter (24.8º versus 18.2º), the authors tentatively discuss banking decreasing risk of injury to the outside limbs.
Figure 2. A: Greyhound racing on curved section of track, B: Forces acting on the dog during cornering (V2/r: centripetal acceleration, a: resultant acceleration, g: acceleration due to gravity (Usherwood and Wilson, 2005).
In figure 2, cornering is shown. The compressive force is directed through the hindlimb, along with centrifugal forces of the turn. Iddion, Lockyer and Frean, (2014) also investigated centrifugal forces through the limb, noting that firmer track surfaces (either due to material or dry weather) are likely to increase injury due to reduced shock
Payne (2013), noted asymmetry in bone density between body sides in racing greyhounds. The author saw thickened right tarsal bones on post mortem. He notes that proper exercise regimens with this one-sided favouring in mind could see gradual, steady adaptation of bones and the musculoskeletal system to reduce incidence of racetrack injury. Marcellin-Little, Levine and Taylor (2005), also discuss the impact that well-conditioned muscle can have on injury. The authors note that well-conditioned dogs are less likely to become lame at fracture and are likely to heal faster. Owing to this, even conditioning of both sides would be beneficial for the athletic patient. As a proportion of overall body mass, greyhounds are noted by Williams et al., (2008) to be 50% muscle, in contrast to horses observed to be 40%, showing the musculoskeletal system as a huge factor to consider for conditioning.
Greatest incidence of dog loss, either through euthanasia or inability to race again, was due to hock injury (Cave, Firth and Thompson, 2011). The authors noted that micro-fractures appeared to develop during training. Research carried out by Schneider, Delfabbro and Burns (2012), suggests future work into racing dog laterality in terms of safety. It was suggested that from an animal welfare perspective, allocating greyhounds to the most suitable starting boxes based on behavioural preferences (including leaning and cutting across), may reduce racetrack collisions and injury. The authors discuss the concept of skilled dogs potentially being able to lead with the preferred limb facilitating most skilled turning and manoeuvring. It is discussed, in agreement with Hackert et al., (2008) that more research is needed to test this hypothesis.
1.4 Study aims and objectives
This study aimed to investigate motor laterality in relation to difference in muscle mass. Information gathered may prove useful in rehabilitation, safety and training for animals, to ensure even conditioning and tone. Monk, Preston and McGowan, (2006) note great importance of building both mass and quality of muscle evenly across all four limbs. This research may improve knowledge on the ability of laterality to influence muscle mass in individuals.
This study investigated if, in the sample tested, dogs that presented with a preferred paw had asymmetry in muscle mass. This was investigated using the following objectives:
- To establish motor preference using the First Step Test (Tomkins, Thomson and McGreevy, 2010).
- To use the lateralisation index to establish strength of preference.
- To take measurements of limbs using an IDASS™ spring tension tape measure and to calculate a mean limb circumference.
- To calculate muscle mass differences between limb pairs.
- To compare findings of strength of laterality and differences in muscle mass to establish if a correlation is present.
1.5 Study hypotheses
Based on knowledge from human, equine and canine literature the following hypotheses were generated (Table 1).
Table 1. Hypotheses for the study.
|Laterality||Dogs will show no lateralisation||Dogs will show lateralisation|
|Muscle mass||There will be no difference in muscle mass on either side||Dogs will have differences in muscle mass on each side of the body|
|Comparisons||There will be no difference in muscle mass between the favoured and non-favoured side||There will be an increase in muscle mass on the favoured side|
The species for study was the domestic dog (Canis familiaris). Initial sample size was n = 20, concurrent with limb circumference research by Smith et al., (2013) and initial First Step testing research by Tomkins, Thomson and McGreevy (2010). One subject was excluded after testing due to ambiguity over unilateral issues. The following breeds were studied;
|Border Collie||(n=2)||Jack Russell||(n=1)|
|Springer Spaniel||(n=1)||Mixed breed unknown||(n=1)|
Mean age of subjects was 4.9±3.16 years. Subject choice was opportunistic (male, n=7, female, n=12).
Building on criteria set out by McGreevy et al., (2010), certain exclusion criteria were applied (Table 2).
Table 2. Exclusion criteria for subjects.
|Missing limbs||All limbs are necessary to allow comparison of muscle mass differences between body sides.|
|Gait abnormality||Includes: unilateral lameness, uneven gait.
Uneven weight distribution may influence muscle mass.
|Past or present limb injury||Potential for increased uneven weight bearing through limbs causing hypertrophy.|
|Arthritis – greater on one side||Due to associated conformational changes in muscle making limbs non comparable.|
It was only possible to exclude dogs with veterinary diagnosed (or owner suspected) illness that were disclosed at the time of study.
2.1 Paw Preference
To establish laterality, First Step testing was used. Set out by Tomkins, Thomson and McGreevy (2010), animals were led down a staircase a total of 50 times. The handler was positioned to the right for 25 repeats and the left for 25 repeats. Side swapping aimed to remove lead side bias that may occur. The first paw used, i.e. to reach and contact the lower step, was recorded as preferred paw for that repeat. Figure 3, shows the clarity of viewing the first paw used when the researcher was positioned correctly.
Figure 3. From Thompson, Tomkins and McGreevy (2010). Clear ability to observe paw choice during the ‘First Step’ test.
A ‘First Step’ recording sheet was drawn up to record first foot for each repeat (also limb measurements). Subjects were offered breaks due to the repetitive nature of the task, and water and treats were available.
2.2 Limb Circumference
In order to ascertain differences in muscle mass between limbs, a spring tension tape measure was used. Figure 4 shows the tape measure, central button (A) is used to retract the tape, creating constant tension around the limb. The right clip (B) holds the end of the tape in place around the limb.
Figure 4. IDASS™ spring tension tape measure. (IDASS, London, UK).
Limb circumference was used to measure human muscle mass by Monteiro et al., (2014) on upper limbs in patients suffering with lymphoedema. The spring tension tape was used to reduce tension related human error present in conventional tapes. Owing to the spring mechanism and clip, standard tension was maintained each time (Millis and Ciupercia, 2015; Smith et al., 2013). Tantua et al., (2014) used a spring tape measure in their human limb circumference studies. They noted its excellence as an inexpensive, straightforward tool for measurement, giving repeatable, reliable results. The authors note the potential for mismeasurement if used inappropriately (i.e. tightened too much). To reduce risk, each measurement was taken 3 times and a mean of the measurements calculated. Geil, (2005) noted spring loaded tape measures to give the most accurate measurements (testing a known circumference) of the 7 measuring tools evaluated, including callipers and standard tapes. Concurrent with Geil, (2005), Sanders and Fatone, (2011) found the spring tension tape to deliver greater accuracy of recording than the standard tape.
Measurements were taken with animals standing, aiming to ensure even weight distribution and muscle tension between limbs (MacDonald, Allen and Monteith, 2013; Gordon-Evans et al., 2011). Circumference measurements were taken at set limb intervals, detailed by Millis and Levine, (2014), as 50% the length of the humorous and femur. This distance was individually variable and established prior to taking measurements.
2.3 Analysis of Data
The ‘Dog Information and Owner Consent Form’ was used for details and consent. All data collected was handled in accordance with the Data Protection Act (1998).
2.3.1 Laterality index
The laterality index calculation (Batt, Batt and McGreevy, 2007) was used to establish the strength of paw preference. A negative value indicated left paw bias, while positive values indicated right bias. Values range from -100 to +100, on a scale of strength, with ±100 being strongest. Values close to 0 indicated ambidexterity.
The laterality index calculation:
|Laterality index =||(R – L) / (R + L)|
Z-scoring was used to determine statistical significance of directional paw usage. This aimed to remove ambiguity and establish a cut off for ambidexterity in subjects. In line with Marshall-Pescini et al., (2013); Schneider, Delfabbro and Burns (2013) and Batt, Batt and McGreevy (2007), a z-score of >±1.98 was considered to be significant. Z = >±1.98 equated to dexterity classification of subjects with LI scores above ±28.
The z-score calculation:
|Z-score =||(R – [(R+L) / 2] / √ [(R+L) / 4))|
2.3.3 Normality and correlations
Normality of data was established by Kolmogorov Smirnov (KS) test using SPSS. Further statistical analysis looked for a relationship between strength of paw preference (+100 to -100) and difference in muscle mass (∆ mm), both of which are continuous scale variables. Parametric data was analysed using a Pearson’s Product Moment correlation.
Data gathered for laterality, z-score, hind difference, fore difference and age was found to be parametric, with P = 0.200 for all variables.
3.1 Laterality Scoring
Table 3 shows the z-scores, laterality index and handedness of subjects. A negative value indicates a left preference (-100 strongest), while a positive indicates right (+100 strongest). The z-score was used to determine statistically significant preference, ≥±1.98 was considered significant, placing subjects into left or right handedness categories.
Table 3. Z-scores, laterality index and handedness of subjects.
3.1.1 Dexterity of dogs, current findings in relation to existing research
Figure 5 shows the proportion of dogs in each Dexterity category, based on Z scoring (ambidextrous, left and right). Findings from this study (striped) have been overlaid with percentages from other published studies of laterality in domestic dogs (1987-present).
Figure 5. Bar chart of dexterity compared to other research, this study represented with striped bar.
3.2 Muscle measurements
The laterality index showed values in negative to indicate the left hand side (i.e. left handed) and positive to show the right hand side (i.e. right handed). To show the muscle increase in a certain direction, ± was used. This study followed the same principles as the laterality index, applying ‘+’ to increased muscle on the right side and ‘-’ to muscle on the left.
This distinction was to enable analysis of muscle in a directional manner. Without direction, it would not have been possible to assess if the animal had an increase on the side of their paw preference or otherwise. Table 4 contains data of limb measurements and differences.
Table 4. Mean measurements of each limb taken for each dog and the increased mass seen on each side.
|Participant Number||Mean Fore (mm)||Mean Hind (mm)||Difference (mm)|
3.3 Hind difference and laterality
Hind difference and laterality showed a statistically significant positive Pearson correlation (r19 = 0.527, P<0.020) (Figure 6).
Figure 6. Graph to show the correlation between hind difference and laterality.
The trend line shown on the graph represents the correlation coefficient 0.527, showing a moderate positive correlation.
3.4 Fore difference and laterality
Testing was carried out between fore difference and laterality. This did not yield a statistically significant Pearson correlation, (r19 = 0.023, P=0.927) (Figure 7).
Figure 7. Graph to show the correlation between Fore Difference and Laterality.
3.5 Age and hind difference
A statistically significant negative Pearson correlation was also found between age and hind difference (r19 = -0.619, P<0.005) (Figure 8).
Figure 8. Graph to show the correlation between age and hind difference.
The trend line shown in figure 8, represents the correlation coefficient of -0.619, a moderate negative correlation.
The purpose of this study was to investigate if there was a relationship between strength of laterality and increased muscle mass in dogs. Laterality was found to be positively correlated with difference in hind muscle mass, but no correlation was found in the forelimbs. A negative correlation was found between subject age and hindlimb muscle mass.
4.1 Laterality and hind difference
A positive correlation between laterality and hind muscle mass was found. Pasi and Carrier (2003) note that in dolichocephalic breeds (including non-racing greyhounds), muscle mass is proportionately higher on the hindlimbs than forelimbs. This is supported by Usherwood, Williams and Wilson (2007) who discuss muscle anatomy being suggestive of locomotor power from the hindlimb, noting additional validation from force plate measurements at trot in dogs (Lee, Bertram and Todhunter, 1999). Fuchs et al., (2014) use the analogy that the hindlimbs are like levers, exerting net propulsive force, powered by hip torque.
Hind power generation is also reported in the equine literature, with forelimbs elevating the forequarters at canter and gallop, there is pelvic rotation and flexion of the sacroiliac junction (Walker et al., 2016; Crevier-Denoix et al., 2013). Hobbs and Clayton (2013) studied horses at trot, observing forelimbs providing greater breaking and lower propulsion, with the hindlimbs seeing the opposite. Figure 9, shows use of the fore and hindlimbs as propulsive and deceleration tools. Forelimbs are shown acting as a break, taking the ground reaction force (GRF), hindlimbs are shown providing upward propulsion.
Figure 9. Diagram of jumping in horses showing limb functions (Powers and Harrison, 1999).
In strongly lateralised quadrupeds, it is possible to speculate greater force being applied through a preferred limb. Human studies by Seeley, Umberger and Shapiro (2008), saw dominant limb propulsive impulse was 7% higher than non-dominant. As a bipedal study this should be interpreted cautiously in relation to quadrupedal locomotion due to the use of only two limbs in locomotion, with 100% of bodyweight carried through the bipedal lower limbs. There is also a lack of separation of structures in bipeds. In the racing greyhound, there is almost complete separation between propulsive muscle and those for bodyweight carriage (Usherwood and Wilson, 2005), whereas the human lower limb is adapted to do both tasks. In a study of military dogs (n=7), Bockstahler et al., (2008) observed compensatory movement patterns occurring through certain joints, with changes to flexion and range of motion attributed to this. In the context of the present study, this may suggest feasibility of seeing increased muscle mass acquired through favouring of one limb. However, the study used dogs with subclinical tendinopathies, so findings are not directly applicable.
In contrast to findings in humans and dogs, equine research carried out by McGuigan and Wilson (2003) and Witte, Knill and Wilson (2004) observed the opposite, with the non-leading limb experiencing the greatest peak vertical GRF. McGuigan and Wilson (2003) recorded leading limbs producing GRF of 9.74 ±1.40N kg–1, with non-lead limbs producing 11.96 ±0.66N kg–1 at canter. Witte, Knill and Wilson, (2004) noted that as speed increased to maximal racehorse running speed (18m/s–1, on treadmill) horse gait became more symmetrical and GRF disparity between sides was greatly reduced.
4.2 Laterality and fore difference
No correlation was found between laterality and fore difference. As mentioned previously, power generation mainly occurs through the hindlimbs, with forelimbs primarily functioning for carriage of the majority of bodyweight, deceleration and manoeuvring (Corbee et al., 2014). Usherwood and Wilson, (2005) discuss muscles for propulsion in the hind being almost completely independent of the weight bearing muscles of the fore during sprinting. Williams et al., (2009) discuss the upwards pitch of the forelimbs during acceleration, noting them to barely contact the ground. In earlier work, it was suggested by Williams et al., (2008), that the forelimbs may have a role in achieving an additional reserve of acceleration when the hindlimbs are at full mechanical capacity. They suggest that the hind joint may not have the scope to support more muscle without limiting joint mobility.
Pasi and Carrier (2003) noted that running breeds (Greyhounds) and fighting breeds (Pit Bulls) exhibit conformational differences. Pit Bulls demonstrated greater or equal cross sectional areas in the forelimbs than hindlimbs, with Greyhounds exhibiting the opposite. Research by Williams et al., (2008) directly contrasts these conformation findings. The authors studied racing Greyhound limbs (n=7) on post mortem, finding that 18.6% (±2.7%) of total body muscle was present on the thoracic limbs with 18.5% (±0.3%) present on the hind limbs. Williams, Wilson and Payne (2007) and Alexander, Dimery and Ker (1985) have discussed the necessity to consider the back as a functional extension of the pelvic limbs in racing Greyhounds due to its role in their elastic spring-like locomotion. Inclusion of the back as part of the pelvic limb, would see the pelvic/hind muscle percentage rise to 30.5% of body mass (Williams et al., 2008).
It is feasible, considering these suggestions, that an increase in fore muscle mass in the subjects selected for this study would not be seen. This sample were not of athletic build, nor ability. Their propulsion is likely to have occurred through the hind without this additional forelimb work, proposed by Williams et al., (2008). In the case of forelimbs, it may be possible to hypothesise that forelimbs would see an increase in directional muscle if the sample were athletic sporting dolichocephalic dogs with the ability to access this fore muscle ‘reserve’.
4.3 Age and hind difference
In this study, a negative correlation was found between age and hind difference. Data showed n = 12 with hind difference of <±10mm, n = 7 had hind difference ≥±10mm. Of the seven, five had a statistically significant z-score (were lateralised), two had LI scores of -20 (±28 was preference cut off) (figure 10).
Figure 10. Hind mass difference and age. Colour has been altered to display lateralised animals (red) and ambidextrous (green). Two circled subjects were ambidextrous with muscle mass difference ≥±10mm.
4.4 Laterality differences between studies
Thompson, Tomkins and McGreevy (2010) proposed that future handedness studies in dogs should follow the First Step testing procedure, owing to repeatability, validity and lack of training influence. Despite this, little canine laterality research has occurred using First Step.
Figure 11 shows the dexterity findings from this study, versus those of Tomkins (2012), also using First Step. The findings of this study contradict those found by Tomkins, (2012). The low number of right pawed dogs is also interesting to compare with human handedness. Approximately 90% of the human population have been found to use their right hand for manual tasks (McGrath et al., 2015; Wells and Allsopp, 2009; Murphy and Arkins, 2008). Wells et al., (2016) aimed to directly compare laterality studies in humans and dogs using the Kong™ test. Interestingly, their findings suggested that holding a Kong™ (in humans, at least) highlighted the non-dominant hand, with participants (76-82%) reporting that they secured the Kong™ with their non-favoured hand before using their mouth to retrieve the piece of paper inside. This raises questions on the validity of use of the Kong™ test in dogs for establishing a dominant limb, when in fact, it may be identifying the non-dominant.
Figure 11. Laterality in this study versus the study of Tomkins (2012), also using First Step, overlaid with human studies for comparison.
A number of studies have used multiple measures for laterality. Wells, (2003) used three tasks, finding lack of consistency in strength and direction between groups. Tomkins, Thompson and McGreevy, (2010) used two tests (including First Step) finding similar results, with both tasks only agreeing for 31% of paw preferences. Both studies agreed that paw preference appears to be labile and task dependent. Lability was also found by Pouydebat et al., (2014) in primates (n=14), observing swapping of preferred hand depending on task (foraging as opposed to swiping). Despite disagreements between tasks, it may be possible, by development of two complimentary tasks, to remove or classify those animals on the borderline of ambidexterity.
4.5 Methodological limitations
4.5.1 Veterinary records
Under the Animal Welfare Act, (2006), owners are legally required to seek veterinary treatment for their animals in illness or injury. Access to veterinary records would allow a brief history of each animal before testing. This would be especially useful in ambiguous cases, or cases lacking owner recall. However, issues with veterinary records have been documented. Robinson et al., (2015) discuss equine practice, finding notes to be variable with 10/28 signalment points differing between practitioners observing the same animals. This may be due to experience or poor record keeping. Werner (2009) notes the importance of standardisation within practice to prevent confusion. Yeates (2012), identified vague terminology within records which may not be understandable on review. The use of veterinary records may have allowed more stringent exclusion criteria to have been applied. For example, they would have given the interval between cruciate ligament surgeries which saw one case excluded and may have allowed better understanding of animals with bilateral orthopaedic conditions.
4.5.2 Breed choice
McGreevy et al., (2010), identified a significant correlation between breed and presentation of two paws simultaneously in a manual task. This was noted especially in whippets (most likely to use two) and pugs (most likely to use one). These presentations were interesting in relation to this study as a range of breeds were used, with one notable presentation of two paws observed. However, the study by McGreevy et al., (2010) used a Kong™ based task, rather than presentation in locomotion, as in the present study. The use of first step may have negated the confounding presentation of two paws at once.
A relationship has been found between breed and laterality in equine studies. McGreevy and Thompson (2006), found a significant left leg preference in Thoroughbreds and Standardbreds but no preference in Quarter Horses. The authors also found more variability in Thoroughbreds, not observing a population bias, instead seeing greater individual differences between subjects. Lack of population bias in Thoroughbreds was contradicted by Williams and Norris (2007), who saw 90% (n=32) lateralised in one direction.
In further research it may be preferable to study one breed to increase internal validity. It was not possible to assess impact of breed on lateralisation in this study due to the mix included (see figure 12).
Figure 12. Graph to show variation in dog breeds (lateralised – striped). Crossbreeds represented by predominant breed.
4.5.3 Sample size
Due to removal of subject 11, sample size fell below 20. For future study, it would be preferable to have more subjects, concurrent with studies such as Tomkins et al., (2012) First Step (n=114), and van Alpen et al., (2005) recording first foot to hit the ground (n=36). Increased sample size would increase external validity and have been more representative of the canine population. A larger sample may have allowed stratification by breed, allowing comparisons to be investigated.
A larger sample may also allow assessment of more variables between dexterity groups, as was the case with Schneider (2012), who drew conclusions between laterality and temperament. This study struggled to draw comparisons as the z-score only identified 3 dogs as right pawed and 6 left, of the 19 tested. This did not give a large enough sample for significant correlations to be investigated without the inclusion of ambidextrous animals.
4.5.4 Full history
There were three cases (subjects 17, 18, 19), for which a full history was not available. All 3 identified as significantly left or right pawed (L=17 and 19, R=18) with directional muscle mirroring preference. These dogs had been adopted from the Dogs Trust as adults and came to the centre without background information. All were health checked by the Dogs Trust vets and declared healthy. Doring et al., (2009) studied fear (shown in 78.5% of studied dogs on entering practice) and presentation of illness. Conditions were found to be presented differently in a state of fear than reported at home. This raises questions of reliability of in-practice check-up of animals prior to rehoming.
4.6 Further research
This study showed a positive correlation between hindlimb muscle mass and laterality. It is not known whether forelimbs and hindlimbs are lateralised in the same direction, or as a diagonal pair. Brown, Zifchock and Hillstrom (2014), studied human footedness and saw preference established by choice when kicking a ball and people advising as to their preferred foot. Self-reporting was also employed by Svoboda et al., (2015). Obviously, there is greater difficulty in assessing hindlimb laterality in animals, as they are unable to self-report and as recordable motor tasks are performed with forelimbs.
Current work by Gough and McGuire (2015) focuses on hind leg lifting for urination as presenting a favoured side. Urination behaviour is sexually dimorphic and this is likely to bias results (Cafozzi, Natoli and Valsecchi, 2012). Although, it was discussed by Wirant and McGuire (2004) that females over 4 years (n=6) directed 70-80% of urine at an environmental target, they did not typically lift their leg, rather preferring to position by leaning.
Gough and McGuire, (2015) aimed to assess males and females using this method. As expected, a large proportion of females (and immature males) did not lift a leg and were therefore excluded from analysis. Unsurprisingly, dogs fitting the criteria for analysis (≥20 leg lifts in walking time) were predominantly males (n=20, females n=2). Cafazzo, Natoli and Valsecchi, (2012) and Pal, (2003) noted females to urinate less than males while free roaming, regardless of inclusion of the leg lifting task, making them less likely to fit the criteria of 20 urinations. Rezac et al., (2011) observed males to be 32% more likely than females to scent mark with urine after another dog had been in the area. This was not controlled in the Gough and McGuire (2015) study, with all dogs walked in a standard area one after another. It is possible to speculate that dogs walked later may have shown greater urination frequency due to marking over other dogs, biasing later subjects for inclusion.
Development of a separate task could be the challenge of future researchers to allow equal assessment of males and females. Perhaps use of force plates to assess which hindlimb experiences greater force on walking or rising from lying may be appropriate. In human research by Dessery et al., (2011), authors found initial stride duration was shorter (from heel off to toe off) when participants started walking with non-dominant leg. Measured with force plates, this could be manipulated to encompass quadrupeds. Force plates to evaluate asymmetric weight bearing (to indicate lame hindlimb) were used in equine studies by Oosterlinck et al., (2011) among others. They allow visualisation of slight force reduction applied or timing of foot placement. A cut off in animal cases, for preference versus lameness would, of course, need to be established.
5.0 Conclusion and Applications
The correlations found between strength of laterality and hind muscle mass (with knowledge of quadruped hind propulsion), may suggest a greater proportion of work being applied through a preferred limb, facilitating a subtle increase in asymmetric muscle. This would require further study to assess potential relationships. Perhaps a longitudinal study of canine subjects demonstrating preferential paws in adolescence, followed up with measurements during life stages could be used, to see whether muscle progression is following that laterality.
The correlation seen between age and hind muscle mass difference is suggestive of an increase in asymmetry during the ageing process. This is to be expected if subtle asymmetry occurs throughout development and is not accounted for in future training (i.e. ‘evening out’ of the muscle and gait). If an animal has been conditioned unevenly throughout its life (due to strong preference for one paw, inappropriate training regime, or otherwise), it is not unreasonable to infer that this may reflect in muscle present in adulthood. Again, further controlled study would be necessary to assess this theme.
External validity could be improved in further study by increasing sample sizes and stratifying sample by breed. Age, whilst uncontrolled, saw a spread of subjects, ranging from puppy (5 months) to senior (10 years 5 months). Perhaps, in further study, this should be controlled for, with either one age range assessed, or a controlled number within each age bracket.
Future research into safety for racing animals could be potentially beneficial for health and welfare. Allocation of animals to racing boxes suiting their laterality and preferences, along with knowledge to condition them accordingly and evenly may see reductions in injury on the racetrack and during training.
A new test, to assess hindlimb laterality may be beneficial in establishing whether forelimbs and hindlimbs follow the same preferential direction, or if a diagonal pair is favoured. Developing a test for hind preference may prove challenging, but is likely to provide valuable information to the canine field.
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