1
Discrimination of human and dog faces and inversion responses in 1
domestic dogs (Canis familiaris) 2
3
Anaïs Racca
1,2
, Eleonora Amadei
1,3
, Séverine Ligout
1
, Kun Guo
2
, 4
Kerstin Meints
2
, Daniel Mills
1
5
6
1
Department of Biological Sciences, University of Lincoln, UK 7
2
Department of Psychology, University of Lincoln, UK 8
3
Dipartimento di Morfofisiologia Veterinaria e Produzioni Animali, Università degli 9
Studi di Bologna, Italy 10
11
12
Corresponding author: 13
Anaïs Racca 14
aracca@lincoln.ac.uk 15
+44(0)1522 895453 16
17
2
Abstract 18
Although domestic dogs can respond to many facial cues displayed by other 19
dogs and humans, it remains unclear whether they can differentiate individual dogs or 20
humans based on facial cues alone and, if so, whether they would demonstrate the face 21
inversion effect, a behavioural hallmark commonly used in primates to differentiate face 22
processing from object processing. In this study we first established the applicability of 23
the Visual Paired Comparison (VPC or preferential looking) procedure for dogs using a 24
simple object discrimination task with 2D pictures. The animals demonstrated a clear 25
looking preference for novel objects when simultaneously presented with prior-exposed 26
familiar objects. We then adopted this VPC procedure to assess their face discrimination 27
and inversion responses. Dogs showed a deviation from random behaviour, indicating 28
discrimination capability when inspecting upright dog faces, human faces and object 29
images; but the pattern of viewing preference was dependent upon image category. 30
They directed longer viewing time at novel (vs. familiar) human faces and objects, but 31
not at dog faces, instead, a longer viewing time at familiar (vs. novel) dog faces was 32
observed. No significant looking preference was detected for inverted images regardless 33
of image category. Our results indicate that domestic dogs can use facial cues alone to 34
differentiate individual dogs and humans, and that they exhibit a non-specific inversion 35
response. In addition, the discrimination response by dogs of human and dog faces 36
appears to differ with the type of face involved. 37
38
Keywords: Preferential looking, Visual paired comparison, Face discrimination, 39
Inversion effect, Dogs 40
3
Introduction 41
Faces convey visual information about an individual’s gender, age, familiarity, intention 42
and mental state, and so it is not surprising that the ability to recognize these cues and to 43
respond accordingly plays an important role in social communication, at least in humans 44
(Bruce and Young 1998). Numerous studies have demonstrated our superior efficiency 45
in differentiating and recognizing faces compared with non-face objects, and have 46
suggested a face-specific cognitive and neural mechanism involved in face processing 47
(e.g. Farah et al. 1998; McKone et al. 2006; see also Tarr and Cheng 2003). For 48
instance, neuropsychological studies have reported selective impairments of face and 49
object recognition in neurological patients (prosopagnosia and visual agnosia) (Farah 50
1996; Moscovitch et al. 1997), and brain imaging studies have revealed distinct 51
neuroanatomical regions in the cerebral cortex, such as the fusiform gyrus, associated 52
with face processing (McCarthy et al. 1997; Tsao et al. 2006). Likewise, 53
behavioural/perceptual studies show that inversion (presentation of a stimulus upside-54
down) results in a larger decrease in recognition performance for faces than for other 55
mono-oriented objects (e.g. Yin, 1969; Valentine 1988; Rossion and Gauthier 2002). 56
Although the precise cause of this so called ‘face inversion effect’ is still source of 57
debate (qualitative vs. quantitative difference between the processing of upright and 58
inverted faces; e.g. Sekuler et al. 2004; Rossion 2008, 2009; Riesenhuber and Wolff 59
2009; Yovel 2009); it is generally associated with a more holistic processing for faces 60
(both the shape of the local features (i.e. eyes, nose, mouth) and their spatial 61
arrangement are integrated into a single representation of the face) than other objects. 62
The face inversion effect is therefore considered as a hallmark for differentiating face 63
from object processing. 64
The capacity for differentiating individuals based on facial cues is not restricted 65
to humans. Using match-to-sample or visual paired comparison tasks, previous studies 66
4
have found that non-human primates (e.g. chimpanzees (Pan troglodytes): Parr et al. 67
1998, 2000, 2006; and monkeys (Macaca mulatta, Macaca tonkeana, Cebus apella): 68
Pascalis and Bachevalier 1998; Parr et al. 2000, 2008; Gothard et al. 2003, 2009; 69
Dufour et al. 2006; Parr and Heinz 2008) other mammals (e.g. sheep (Ovis aries): 70
Kendricks et al. 1996; heifers (Bos Taurus): Coulon et al. 2009)), birds (e.g. budgerigars 71
(Melopsittacus undulatus): Brown and Dooling, 1992), and even insects (e.g. paper 72
wasps (Poliste fuscatus): Tibbetts 2002) could discriminate the faces of their own 73
species (conspecifics), based on visual cues. Although it is not clear whether face 74
processing in non-human animals share a similar neural mechanism as that in humans, 75
some behavioural studies have noticed a face inversion effect, at least towards 76
conspecific faces in chimpanzees (e.g. Parr et al. 1998), monkeys (e.g. Parr et al. 2008; 77
Parr and Heinz 2008; Neiworth 2007; see also Parr et al. 1999) and sheep (Kendrick et 78
al. 1996), suggesting that a similar holistic process may be used for face perception by 79
these species. 80
Many studies have suggested that the development of a face-specific cognitive 81
process relies heavily on the animal’s extensive experience with certain type of faces. 82
For instance, human adults have difficulties at recognizing faces from a different ethnic 83
group and demonstrate weaker holistic processing towards these faces (O’Toole et al. 84
1994; Tanaka et al. 2004). This so called ‘other-race effect’ can decrease and even 85
reverse by experiencing another ethnic face type (e.g. Elliott et al. 1973; Brigham et al. 86
1982; Sangrigoli et al. 2004). Furthermore, humans and some non-human primates 87
present abilities of discrimination and/or an inversion effect toward faces of other 88
species, provided that they have been frequently exposed to them (generally tested with 89
other-primate species) (Parr et al. 1998, 1999; Martin-Malivel and Fagot 2001; Pascalis 90
et al. 2005; Martin-Malivel and Okada 2007; Neiworth et al. 2007; Parr and Heinz 91
5
2008; Sugita 2008). Finally, human performances in simple human-face identification 92
task are known to depend primarily on the amount of preceding practice (Hussain et al. 93
2009). Taken together, exposure seems to be an important determinant for holistic face 94
processing. 95
Given their long history of domestication (estimated at 12,000-100,000 years 96
ago, Davis and Valla 1978; Vilà et al. 1997) and intensive daily interaction with humans, 97
pet domestic dogs could be a unique animal model for the comparative study of face 98
processing. Despite their extraordinary capacity for discriminating olfactory cues (e.g. 99
Schoon 1997; Furton and Myers 2001), domestic dogs also process visual inputs 100
efficiently. Although they could have less binocular overlap, less range of 101
accommodation and colour sensitivity, and lower visual acuity (20/50 to 20/100 with 102
the Snellen chart) compared with humans, they in general have a larger visual field and 103
higher sensitivity to motion signals (for a review see Miller and Murphy 1995). 104
Growing evidence has revealed that they can rely on facial cues for social 105
communication. They can display a range of facial expressions and these are believed to 106
be important in intraspecific communication (e.g. Feddersen-Petersen 2005). They also 107
attend to and use human facial cues. For instance, they attend to human faces to assess 108
their attentional state (Call et al. 2003; Gácsi et al. 2004; Viranyi et al. 2004) or in 109
problem solving situations (Topál et al. 1997; Miklósi et al. 2003). They are particularly 110
efficient at reading and understanding some human directional communicative cues, 111
such as following human eye/head direction to find hidden food (e.g. Miklósi et al. 112
1998; Soproni et al. 2001), and even exceed the ability of some non-human primates in 113
such tasks (e.g. Povinelli et al. 1999; Soproni et al. 2001; Hare et al. 2002). In a recent 114
study, Marinelli and colleagues (2009) observed the apparent attention of dogs while 115
looking at their owner and a stranger entering and leaving a room. They showed that the 116
