Family dogs are amongst the most popular pets worldwide (1, 2) with a considerable economical and personal impact on human societies. Whilst there is a growing body of knowledge about dog behaviour and cognition (3), the veterinary conditions paralleling human psychiatric disorders are vastly understudied, despite the fact that the dog has been suggested to suffer from many human-like diseases (4, 5). The few studies focusing on this research line include evidence on the presence of symptoms resembling Obsessive Compulsive Disorder (6, 7), Attention Deficit Hyperactivity Disorder (N (8)) and autism (9, 10). These results, however, are of studies from recent years only and do not go beyond a couple of papers. This is especially surprising, since behavioural problems are often reported by owners as those most devastating for every-day life and well-being (11), and unwanted behaviours are amongst the most common reasons for relinquishing dogs to animals shelters (12). Perhaps not surprisingly, in addition to aggressive behaviours (which are the leading reason for animal relinquishment to shelters) other – not directly harmful – behaviours such as being afraid of various things, demanding too much attention and being disobedient are commonly mentioned by owners as a reason to get rid of their dogs (12). Cognitive / psychiatric-like symptoms, amongst which the most commonly studied one is canine cognitive dysfunction, are also perceived as an increased burden by dog owners (13). This in addition to the fact that such conditions prevent the caregivers from living a full life, constitutes a serious animal welfare issue as long as they cannot be properly treated and / or prevented. The present study aims to give empirical data on the currently available behavioural tools to measure one such human-like condition, namely the behavioural pattern resembling hemispatial neglect.

Recently it has been suggested (14) that dogs’ side bias behaviour, which is often reported in cognitive experiments, shows parallels to human hemispatial neglect. The psychiatric condition of hemispatial neglect is characterised by a deficit in attention to and awareness of the contralesional hemispace following a brain injury (15). The behavioural manifestation of unilateral spatial neglect in everyday life includes the patient bumping into objects on the neglected side, ignoring the food on one side of the plate, difficulties in dialling numbers, watching TV, playing social games and not responding to people situated on their neglected side. There are also a couple of documented cases of dogs showing hemispatial neglect including a citizen science example published on a personal blog¹ where the dog ignored food on half of the plate, as well as a veterinary case study (16) where the dog only responded to stimulation coming from one side. The study of Bolló et al. (14) applied a spontaneous two-way-choice task, and tested a group of dogs with previous side bias history (they had previously shown 100% bias to left or right in other two-way choice tasks). It was found that the majority of the subjects retained their side bias suggesting that the phenomena is stable across time and situations. Furthermore, dogs relied on an egocentric reference frame in their choices, similarly to human patients.

Whilst these indirect parallels are an important first step, there are still methodological problems that prevent the application of such behavioural tests in veterinary practice. First and foremost, to date there is no direct comparison between dogs and humans’ neglect-like behaviour. In human patients, hemispatial neglect is typically assessed via paper and pencil methods, such as the clock-drawing task (17), line bisection or the cancellation test (18). In these cases, human subjects have to make a drawing, or cross out certain objects in an array of distractors. These tests are obviously not compatible with dogs’ motor skills. There has been an effort to develop a visuo-spatial search task matching the cancellation test that can be performed with dogs (19); this is essentially a food detection task with a grid of possible hiding places and was successfully implemented by the authors.

A further problem with the veterinary applicability of testing human-like psychiatric conditions in dogs, is that standardised information regarding the normal range versus the pathological dog behaviour is mostly lacking see, e.g., Csibra et al. (20) for a similar argument. Thus in addition to the approach used in Bolló et al. (14) tests need to be performed on healthy subjects as well.

It is important to note that hemispatial neglect is a debilitating condition making human patients’ everyday life more challenging due to patients failing to notice objects or people on one side (15) and thus having difficulties, e.g., crossing the road or navigating in the environment. An important criteria for side bias in dogs is that it leads to disadvantageous choices: subjects with a side bias receive less food reward in cognitive tests. For example in a pointing-following test (21) where dogs generally perform above chance (receiving a food reward for “good” choices, and receiving no reward for “bad” choices), subjects with a side bias will perform merely at chance. This differentiation needs to be made from behavioural and brain lateralisation – a natural phenomenon wide-spread throughout the vertebrate taxa (22) –, which on the contrary is argued to have adaptive functions. There is also ample literature on dogs’ lateralised response to different (e.g., emotional) stimuli (23), which again is a research line different from disadvantageous attentional biases.

In the current paper we first aim to test whether humans’ performance in the validated pen and paper cancellation tests matches the visuo-spatial search task claimed to be the canine cancellation test. Next we will test dogs in both the canine cancellation (visuo-spatial search) task as well as in two-way choice tests where parallels between dog side bias and human hemispatial neglect had been shown.

The current study tested different visuo-spatial tasks in both dogs and humans with the aim of establishing a comparative framework to study hemispatial neglect-like side biases. Our findings are mixed regarding the reliability and potential veterinary application of the tasks tested. We have found that both canine tasks are easy to administer – and are thus suitable for the use in veterinary settings. However, a study involving more subjects (both healthy as well as post-stroke dogs) would be needed to establish standard thresholds for veterinary diagnosis. An additional important finding is that dogs’ first choice in the two-way choice task and human’s first choice in the visuo-spatial task is a significant predictor of total “left” choices. This means that the tests could potentially be shortened to a single trial each, which would further ease their administration in veterinary settings. This is in line with findings on other species (e.g., cats: (26)) as well. We should note, however, that for the visuo-spatial tasks no significant association was found between first choice and total score in case of dogs. Whilst this is likely due to the predominant “middle” first choices (and thus the low subject numbers for left versus right choice), the test needs to be carried out on a larger sample (with more left- and right first-choosers) before the validity of the first choice can be confirmed.

In humans we have shown, as expected, that healthy young subjects perform at ceiling in paper & pencil cancellation tests used with clinical patients. The tests (‘Apples’ test and ‘Bells’ test) still yielded meaningful data with between-individual variability when focusing on the side-bias aspect of the responses. The ceiling performance of healthy subjects in a test designed for neglect patients is not surprising as they were given the same time to complete the search. For the present analysis we only used subjects’ first few answers, which is essentially equal to a stricter time limit if we consider the remaining targets as omissions. Using this method, subjects’ left bias in the two paper & pencil tasks were significantly related confirming that these are reliable measures. The left bias found in the present study confirms previous reports of human cancellations tests (27, 28), meaning that in paper and pencil tests subjects find stimuli on the left first. This pattern presumably aligns with the left-to-right reading direction, although findings on, e.g., Arabic populations are mixed: some did find a right bias in visual scanning, as would be expected based on the reading direction (29), but others studying Arabic subjects (30) found a left bias similar to our finding, although only in the 63% of the subjects, which is lower compared to the present results (‘Apples’ 84%, ‘Bells’ 91%). Yet others (31) have found bidirectional search patterns in bilingual subjects with one language reading from left to right, whereas the other language reading from right to left. Illiterate subjects have been shown to manifest a disorganised visual search strategy (32). So taken together it does seem that culturally learned reading direction influences search pattern in paper and pencil cancellation tests. On the other hand, performance in the visuo-spatial task (which was designed to mimic the dog version of the cancellation test) was not related to performance in either of the paper & pencil cancellation tests. However, considering subjects’ left biases in the ‘Apples’ and ‘Bells’ tests this finding does not invalidate the visuo-spatial search task, which was free from such a strong left bias and showed a more even distribution between left and right searches as could be expected from healthy subjects.

For the dog subjects we also found a near-ceiling search performance with meaningful variance in their left / right biases. Furthermore, no relationship was found between left bias in the two-way choice task versus the visuo-spatial search task. This suggests that the two tests measure different aspects of side bias and spatial cognition, despite the fact that both had been validated to some extent. Spontaneous two-way choice tasks have been shown to be a reliable measure of side bias (14), and they have also been used to confirm magnetic alignment in dogs (33). The visuo-spatial search task was shown to be related to left / right paw use in a Kong test (19). Dogs’ paw preference was not assessed in the present paper – mainly because dogs used their muzzles / full body to complete their task, so paw preference was not a direct confounding factor for the outcome measure. Thus based on the current dataset we cannot provide results for or against the relationship between visuospatial attention and paw preference. It is important to note, however, that the wide variety of available tests measuring such motor laterality in dogs (e.g., paw that the dogs give on command, paw used to hold a chew or a Kong, paw preference during locomotion or when stepping on the stairs, etc) have been shown to yield inconsistent results across tasks (34). Thus these test likely measure slightly different forms of motor laterality, and at least some of these can potentially be related to the here used side bias tests – e.g. head turning responses (35) or paw used to remove an adhesive tape from the nose (36) might relate to variability in muzzle use which future research applying the current tests needs to take into account. The results of the present study align nicely with the inconsistencies reported on other species and across tasks (37–39), as it was similarly found that the two side bias measures currently investigated in dogs were not related. It is further argued (40) that task complexity and other factors related to the specific testing situation (e.g., tastiness of the item to be retrieved) also affect lateralized behaviour.

Here we found that dogs’ side bias in the visuo-spatial task is influenced by their age and sex. This further argues for the validity of the test, since old dogs have been previously shown to be more prone to develop side bias (41). The effect of sex was in the opposite direction compared to previous reports on paw preference (36, 42), as we found that females were more left-biased, as opposed to the right paw-preference reported. Others (e.g., (43–45)), however, have not found any sex-differences in laterality.

Despite behavioural parallels between human hemispatial neglect and dog side bias (e.g., (14)) the underlying brain mechanisms are likely to differ in the two species. It has been shown for example in an fMRI based study that lexical processing in dogs is localised in the right hemisphere, contrary to humans (46). Such brain level differences, however, do not invalidate the use of animal models in psychiatric research, and dogs are continuously considered as a valid parallel to human neuro-cognition (47).

A further point to be considered for the here presented results is that due to the method validation aspect of the current study, it involved healthy subjects (both dogs and humans). For humans it has been reported, that – as in case of most psychiatric disorders – there is a continuum between unilateral spatial neglect symptoms and normal behaviour (48). The so called pseudoneglect has been described in clinically healthy patients, being a mild form of sidedness, manifesting, e.g., in bumping into objects on the left side with a greater probability than on the right side (49). This sub-clinical attentional bias has also been connected to, e.g., eye-blink rate in humans (50). Such connections are yet to be established between neurologically healthy dogs with side bias and post-stroke dogs showing hemispatial neglect symptoms.

In conclusion, we have shown here, that an easy to carry out behavioural test, such as the visuo-spatial search task used here, can be used to detect individual differences in dogs’ (and humans’) side-bias. Since the currently studied subjects were all neurologically healthy, further research needs to determine if such individual differences underlie, e.g., predisposition for hemispatial neglect-like symptoms later on. Additionally the treatment and prognosis – known to vary considerably in case of human neglect patients (51) – needs to be studied in dogs as well.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving humans were approved by National Research Ethics Committee, Research Ethics Committee of Eötvös Loránd University. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study. The animal studies were approved by National Animal Experimentation Ethics Committee. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent was obtained from the owners for the participation of their animals in this study.

AK: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Supervision, Visualization, Writing – original draft, Writing – review & editing. ER: Formal analysis, Investigation, Writing – review & editing. HB: Conceptualization, Methodology, Supervision, Writing – review & editing. JT: Conceptualization, Funding acquisition, Methodology, Supervision, Writing – review & editing.