Review
Canis familiaris As a Model for Non-Invasive Comparative Neuroscience

https://doi.org/10.1016/j.tins.2017.05.003Get rights and content

Trends

A shared social environment with humans, cooperativeness, trainability, and advances in awake and non-invasive measurement of neural processes make the domestic dog a promising model of human neurocognition, one that complements traditional models.

For the dog to contribute to comparative neuroscience in a relevantly comparative, reliable, and valid manner, methods that allow functional comparability to human methods are crucial.

Differences between breeds and species as well as between the designs of canine and human studies confer both methodological advantages and disadvantages.

Dogs permit examination not only of a range of sociocognitive skills that share key behavioral and functional characteristics with those of human, but also of the within-species (i) relationship between brain structure and function, (ii) the effects thereof on neurocognition, (iii) within-subject temporal stability of neural measures, and (iv) correspondence of neural correlates with performance across social, emotional, and cognitive paradigms.

There is an ongoing need to improve animal models for investigating human behavior and its biological underpinnings. The domestic dog (Canis familiaris) is a promising model in cognitive neuroscience. However, before it can contribute to advances in this field in a comparative, reliable, and valid manner, several methodological issues warrant attention. We review recent non-invasive canine neuroscience studies, primarily focusing on (i) variability among dogs and between dogs and humans in cranial characteristics, and (ii) generalizability across dog and dog–human studies. We argue not for methodological uniformity but for functional comparability between methods, experimental designs, and neural responses. We conclude that the dog may become an innovative and unique model in comparative neuroscience, complementing more traditional models.

Section snippets

Animal Models in Comparative Neuroscience

Animal model research is grounded in the idea that animals share behavioral, physiological, and other characteristics with humans. One benefit of such research is increased understanding of phenomena that cannot be directly studied in humans or without cross-species comparison. Neuroscience research into sociocognition has been extended from traditional primate and rodent models to the domestic dog – an alternative and complementary model that permits non-invasive measurement of behavior and

Animal Models for Comparative Cognitive Neuroscience

A goal of comparative research is to establish principles of proximate and ultimate causation (see Glossary) via between-species comparisons and the study of individual organisms. Primary animal models for comparative cognitive science include avian 3, 4, 5, rodent, and primate species [2]. The advantages of rodents include feasibility of handling the animals under laboratory conditions, cost-efficiency, and utility in preclinical and clinical studies [6]. The advantages of primates include

Differences in Skull Formation and Brain Anatomy

The extent of variation in skull formation and brain size is relatively minor among humans: the average female brain volume is 90% that of the male [14], and the average brain volume of a child aged 7–11 years is 95% of the volume of a sex-matched adult [15]. Conversely, there are large differences between dogs in skull shape and size, as well as in brain anatomy. Canine skull length ranges from 7 to 28 cm [16] (i.e., the shortest dog skull is 25% of the longest), making Canis familiaris the

Within-Species Differences in Skull Formation and Brain Anatomy

These within-species variabilities (Figure 1) are relevant for normalization. In fMRI research, the advantages of normalization are that when a set of coordinates is referenced the location to which those coordinates correspond is known, and the results can be generalized to a larger population, compared across studies, and averaged across subjects for group-level analyses. The disadvantages are that it reduces spatial resolution and increases probability of errors in the identification of

Between-Species Differences in Skull Formation, Brain Anatomy, and Physiology

Although further research is needed concerning the degree to which the anatomical structures and circuits of dogs correspond to those of humans, the knowledge that is available is encouraging. There is evidence for correspondence between the species in, for example, primary sensory areas and associated functions [33]. Nevertheless, it is largely unknown whether other areas, especially the frontal and prefrontal cortex, are similarly organized – notably with regard to subdivisions – in a manner

Ethics and Safety

As noted, a main advantage of dogs is that, because they are domestic animals, they can be tested without any need for laboratory breeding, raising, and maintenance. As such, a focus on family dogs makes the dog model ethically permissible. Nevertheless, as aptly discussed by others [1], care should be exercised that no harm is caused, for example that scanner noise and high sound pressure levels do not lead to discomfort and hearing damage, or that RF specific absorption rates (SAR) do not

Concluding Remarks

There has been a notable recent increase in canine neuroscience studies, necessitating the establishment of methodological guidelines and standardization to inform the next generation of studies in this area. We have discussed the foremost questions related to methodology and experimental design in the canine neuroscience literature. As a result, we were able to identify crucial areas for further empirical inquiry. Capitalizing on advantages of the dog as a research model, such as its

Acknowledgments

During the preparation of this article, N.B. and M.G. were supported by the National Research, Development and Innovation Office (grant 115862 K); A.A., A.M., and M.G. were supported by the Hungarian Academy of Sciences (grant F01/031); A.A. was additionally supported by a Hungarian Academy of Sciences Bolyai Scholarship and by the Hungarian Scientific Research Fund (grant OTKA PD116181); and A.K. was supported by Nestlé Purina and the BIAL Foundation (grant 169/16). We thank Árpád Dobolyi and

Glossary

Basilar axis
the axis corresponding to the base of the skull.
Brachycephalic
short-skulled
Calvaria
the bone that covers the cranial cavity containing the brain, in other words the skullcap.
Continuous electroencephalography (EEG)
continuous measurement of electrocortical signal, in other words not a measurement of change in the signal in response to a stimulus.
Cribriform plate
a structure that forms the caudal boundary of the nasal cavity.
Dolichocephalic
long-skulled.
Event-related potential (ERP)

References (107)

  • N. Bunford

    Threat distractor and perceptual load modulate test-retest reliability of anterior cingulate cortex response

    Prog. Neuropsychopharmacol. Biol. Psychiatry

    (2017)
  • O. Muzik

    Statistical parametric mapping: assessment of application in children

    Neuroimage

    (2000)
  • G. Grabner

    A study-specific fMRI normalization approach that operates directly on high resolution functional EPI data at 7 Tesla

    Neuroimage

    (2014)
  • T.J. Howell

    Development of a minimally-invasive protocol for recording mismatch negativity (MMN) in the dog (Canis familiaris) using electroencephalography (EEG)

    J. Neurosci. Methods

    (2011)
  • T.J. Howell

    Auditory stimulus discrimination recorded in dogs, as indicated by mismatch negativity (MMN)

    Behav. Processes

    (2012)
  • D.H. Loewy

    The mismatch negativity to frequency deviant stimuli during natural sleep

    Electroencephalogr. Clin. Neurophysiol.

    (1996)
  • R. Näätänen

    The mismatch negativity (MMN) in basic research of central auditory processing: a review

    Clin. Neurophysiol.

    (2007)
  • D.H. Spodick

    Survey of selected cardiologists for an operational definition of normal sinus heart rate

    Am. J. Cardiol.

    (1993)
  • K. Murphy

    Resting-state fMRI confounds and cleanup

    Neuroimage

    (2013)
  • M.N. Coutanche et al.

    The advantage of brief fMRI acquisition runs for multi-voxel pattern detection across runs

    Neuroimage

    (2012)
  • M. Falkenstein

    ERP components in Go/Nogo tasks and their relation to inhibition

    Acta Psychol.

    (1999)
  • M.G. Wheaton

    Perceptual load modulates anterior cingulate cortex response to threat distractors in generalized social anxiety disorder

    Biol. Psychol.

    (2014)
  • Z. Sümegi

    Emotional contagion in dogs as measured by change in cognitive task performance

    Appl. Anim. Behav. Sci.

    (2014)
  • J. Vas

    Measuring attention deficit and activity in dogs: a new application and validation of a human ADHD questionnaire

    Appl. Anim. Behav. Sci.

    (2007)
  • Á. Erdőhegyi

    Dog-logic: inferential reasoning in a two-way choice task and its restricted use

    Anim. Behav.

    (2007)
  • Á. Miklósi

    A simple reason for a big difference: wolves do not look back at humans, but dogs do

    Curr. Biol.

    (2003)
  • J.W. Pilley et al.

    Border collie comprehends object names as verbal referents

    Behav. Processes

    (2011)
  • A.M. Thompkins

    Functional magnetic resonance imaging of the domestic dog: research, methodology, and conceptual issues

    Comp. Cogn. Behav. Rev.

    (2016)
  • G.S. Berns et al.

    Why did the dog walk into the MRI?

    Curr. Dir. Psychol. Sci.

    (2016)
  • H. Prior

    Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition

    PLoS Biol.

    (2008)
  • T.F. Vandamme

    Use of rodents as models of human diseases

    J. Pharm. Bioallied Sci.

    (2014)
  • K.A. Phillips

    Why primate models matter

    Am. J. Primatol.

    (2014)
  • C. Jennings

    Opportunities and challenges in modeling human brain disorders in transgenic primates

    Nat. Neurosci.

    (2016)
  • D. Papoti

    An embedded four-channel receive-only RF coil array for fMRI experiments of the somatosensory pathway in conscious awake marmosets

    NMR Biomed.

    (2013)
  • Á. Miklósi

    Dog Behaviour Evolution and Cognition

    (2014)
  • G.J. Siegle

    Beyond depression commentary: wherefore art thou, depression clinic of tomorrow?

    Clin. Psychol. Sci. Pract.

    (2011)
  • V.S. Caviness

    The human brain age 7–11 years: a volumetric analysis based on magnetic resonance images

    Cereb. Cortex

    (1996)
  • P. McGreevy

    A strong correlation exists between the distribution of retinal ganglion cells and nose length in the dog

    Brain. Behav. Evol.

    (2003)
  • T. Roberts

    Human induced rotation and reorganization of the brain of domestic dogs

    PLoS One

    (2010)
  • J.J. Schoenebeck et al.

    The genetics of canine skull shape variation

    Genetics

    (2013)
  • A.M. Dickie et al.

    The effect of obliquity on the radiographic appearance of the temporomandibular joint in dogs

    Vet. Radiol. Ultrasound

    (2001)
  • T. Schwarz

    Radiographic anatomy of the cribiform plate (lamina cribosa)

    Vet. Radiol. Ultrasound

    (2000)
  • M. Gacsi

    Effects of selection for cooperation and attention in dogs

    Behav. Brain Funct.

    (2009)
  • R. Kanai et al.

    The structural basis of inter-individual differences in human behaviour and cognition

    Nat. Rev. Neurosci.

    (2011)
  • G.S. Berns

    Functional MRI in awake unrestrained dogs

    PLoS One

    (2012)
  • G.S. Berns

    Replicability and heterogeneity of awake unrestrained canine fMRI responses

    PLoS One

    (2013)
  • P.F. Cook

    One pair of hands is not like another: caudate BOLD response in dogs depends on signal source and canine temperament

    PeerJ

    (2014)
  • D.D. Dilks

    Awake fMRI reveals a specialized region in dog temporal cortex for face processing

    PeerJ

    (2015)
  • M.V. Kujala

    Reactivity of dogs’ brain oscillations to visual stimuli measured with non-invasive electroencephalography

    PLoS One

    (2013)
  • H. Törnqvist

    Visual event-related potentials of dogs: a non-invasive electroencephalography study

    Anim. Cogn.

    (2013)
  • Cited by (73)

    View all citing articles on Scopus
    View full text