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Why Do Dogs Yawn? The Neuroscience Of Empathy & Emotional Contagion - Simply Behaviour - Applied Behaviour Analysis

Why Do Dogs Yawn? The Neuroscience Of Empathy & Emotional Contagion

After a recent research project into the neuroscience of behaviour and a talk given at the ISCP, INTER Dogs and Dog Alliance (see recorded webinar) Introduction To the Science Of Behaviour (Beginners) Seminar we became interested in the concept of emotional contagion and what this means to dogs. To find out more about the neural mechanisms of this concept and what the current research is saying we have a 7 day course. This can be found at:  Emotional Contagion & Empathy, The Neural Mechanisms & Evidence In Dog Behaviour. A lot of people ask us why dogs yawn. Behaviour persons often interpret this as an an early sign of discomfort related to the antecedents in proximity. This is nicely explained in our ladder of aggression below (part of the Essential Training Resource Guide poster pack) Please note you can buy the emotional and essential courses together in a 2 for 1 offer using code GroupVets. These posters look great displayed in professional organisations that really care about getting the right message out to dog owners about safety and behaviour. Universities use our ladder for helping to teach their students.

So, what did we find out about the reasons dogs yawn?

The notion of affective neuroscience relating to the common interpretations of body language have become a subject of interest and we want to try to explore each aspect of “behaviour output”, to give us a further understanding of the internal environment of our animals, what structures are in the brain and how they function in relation to behaviour- based on the evidence.

It was thought that yawning came from a signal going to the hypothalamus, which detected a raise in body temperature and that the yawn acts to cool the brain. This is the thermo-regulation hypothesis. We touched on a social hypothesis too, which is the one that we are currently following. The evidence for the previous is not conclusive. So, here is the story so far….

A yawn lasts for 3-6 seconds and occurs across many species of animal, such as; fish, birds, dogs, chimps and of course humans. It is characterised by a brief period of apnea (a suspension of external breathing). Since around the 4th century BC (Hippocrates) scholars thought yawning had the function of removing “bad air” from the lungs and increasing oxygen circulation in the brain (Trautmann, 1901; Schiller, 2002; Matikainen and Elo, 2008).

It would seem that current studies that look at yawning are lacking in what we actually define as a yawn. Do they come from Physiological and/or metabolic mechanisms and how conserved is this among animal species? How conserved is the function of yawning? It is found that we can completely suppress a yawn (humans). Can animals do this and what are the behavioural, physiological and social consequences? We have not been able to accurately measure how brain oxygenation is affected by yawning (the experiment would be dangerous for humans). This hypothesis is still to be confirmed. How does yawning effect brain metabolism and neurophamacology? What is the effect of middle ear pressure change and does this increase rate of yawning? How are the structures and functions of the paraventricular nucleus of the hypothalamus (PVN) and the neurons in the medulla involved in creating yawning? Is yawning a social synchronising behaviour and how does this occur?

Is it a calming signal?
It is popular to explain yawning in terms of calming signals. Steven Lindsay set out to test the hypothesis that yawning and or licking produces a calming effect in dogs. The results show that this was without consistent effect. They did find that some dogs did respond to human licking and actually licked back in return. Others averted their gaze/head and/or backed away. Some yawned in response to licking actions. This raises the possibility that signals could be producing a mildly aversive response with the dogs. Petting dogs can produce a calming effect of varying strength. The conclusion from this was that caution should be exercised when we suggest that these signals are calming, particularly when it is used without due consideration to context.

The neuroscience bit:
Yawning involves an interaction between the Paraventricular nucleus (PVN) of the Hypothalamus with various hormones and neurotransmitters such as Dopamine, Glutamate, Nitric Oxide (NO) & Oxytocin. Stimulation in this area leads to increased yawning via Oxytocinergic projections in the Hippocampus pons/medulla oblongata. Acetylcholine (ACH), Serotonin, Adrenocortocotrophic Hormone (ACTH) and related peptides use other pathways. Opiods are found to inhibit yawning.

Argiolas et al 1985,1988,1995, 2000 showed that administration of Oxytocin, Dopamine D2 Agonist, ACTH, alpha-MSH (melanocyte stimulating hormone) in the PVN lead to an increase in penile erection and yawning. CRH (corticotrophic releasing hormone) also activated yawning.

Oxytocin in the PVN has two different routes. The Magnocellular which is where Oxytocin is synthesised in the Neurohypophyseal area (where hormones are synthesised and stored for systemic administration throughout the circulation) and axons here serve the posterior pituitary. Then the Parvocellular Caudal, lower brain stem area which has the descending axons to the motor pathways and the Vagus nerve (this is the nerve responsible for our gut instinct and control of our sympathetic flight or fight responses- aka stress) & spinal chord. Activation of the Parvocellular area increases sexual arousal and yawning. How these effects bring about yawning is not yet understood.

Image courtesy of Kita I, Yoshida Y, Nishino S. Sleep and Circadian Neurobiology Laboratory, Center for Narcolepsy, Department of Psychiatry and Behavioral Sciences, Stanford University. USA- From Their paper on sexual arousal and yawning in oxytocinergic pathways.

yawning

Arousal theory:
Walusinski and Deputte, 2004; Matikainen and Elo, 2008; Vick and Paukner, 2010) suggested that yawning might be responsible for the homeostatic regulation of vigilance and brain arousal level. However, yawning does not produce an arousal. Arousal is defined as a global activation of brain activity and it progresses from the brain stem to the central autonomic nervous system and across the cortical areas (Moruzzi and Magoun, 1949; Sforza et al., 2000).

Ear and Air Pressure relief:
Yawning equalises air pressure in the middle ear with the pressure outside. This relieves discomfort in environments where the altitude changes (such as flying). The tensor tympani & stapedius muscles contract and relax when yawning occurs, this opens the eustachian tubes and the tympanal cavities open. This hypothesis gave rise to the explanation of yawning being a way to relieve air trapped in the ear (Laskiewicz, 1953). Middle ear pressure change needs to be further understood and whether this increases rate of yawning.

Deborah Custance & Jennifer Mayer from Goldsmiths College London explored the concept of emotional contagion. Contagious yawning is by far the most reasonable explanation to date. This experiment was designed to take this one stage further and to see if dogs actually had empathy when their owners were in emotional distress. They tested 18 dogs at home and got the owners and strangers to carry out a range of tasks. They filmed the process. They found that dogs would respond to the emotional state of people, when they were upset. They seemed to be able to gauge this from a relatively inert noise (used as a control).

Sauer & Sauer in 1996 recognised synchronisation in Ostriches that were in a group. So, even though this contagious yawning has been identified among many species of animals, the function, development & mechanisms of this are still unclear. Between humans and dogs we are not sure if this shows empathy or not. Human children do not develop empathy-related behaviours until about 4 years old. Madsen, Alenkar, Persson Et al 2013 examined to see if contagious heterospecific yawning occurs when there is attachment history, using heterospecifics. They used orphaned chimps who were fostered by human mothers. It was found that yawning was more contagious than any other postural congruence behaviours in young but not infants and that there seemed to be a developmental aspect to this contagion and that the emotional/social modulatory effect emerges later and is relatively limited to interactions with conspecifics rather than heterospecifics.

Deputte et al showed that yawning occurs to signal moderately unpleasant, socially mild and not immediate threatening situations. There is an area of the brain responsible for the representation of this type of behaviour (Mirror Neuron System- MNS) Evidence for its use as a survival mechanism in group/social communication comes from studies with people who have Autism or Schizophrenia- they do not respond to social cues & yawning.

Brain regions associated with contagious yawning:
Contagious yawning activates the right posterior inferior frontal gyrus which is part of the mirror neuron system responsible for action observation and imitation (Rizzolatti
and Craighero, 2004).
Subjects watching other persons yawn specifically activates regions that are part of a network responsible for empathy and social behaviour (Saxe et al., 2004; Carrington and Bailey, 2009):
The bilateral posterior cingulate (PC, Platek et al., 2005),
The bilateral superior temporal sulcus (STS, Schurmann et al., 2005)
The bilateral ventromedial prefrontal cortex (VMPFC, Nahab et al., 2009)

Image courtesy of studyblue.com

brocas area4

Rizzolatti 2004 looked at the MNS which is responsible for imitation behaviour. It is found in the right posterior inferior frontal gyrus. Aronoff 2009 looked at contagious yawning and movement observation which were all activated in this system which shows empathy and social behaviour in this complex neural network. Haker H1, Kawohl W, Herwig U, Rössler W. Used FMRI to measured neuron activity during contagious yawning.

Bonne Beerda, Matthijs B.H Schildercorrespondence, Jan A.R.A.M van Hooff Et al Studied stress responses in dogs to various aversives. They observed that dogs with very low posture indicated intense acute stress and this is represented in their saliva cortisol responses. In a social setting it was observed that they showed increased restlessness, oral behaviours, yawning etc. Unfortunately, because of the non-specific character of canine heart rate responses, they could not factor this in to the interpretation and its role in acute stress.

We certainly need to do more research into the MNS in dogs. We need to get Greg Burns to invite his FMRI trained dogs back into the lab and see how their Brodmann’s area responds to con-specific and hetero-specific contagious yawning and empathy type behaviour. This MNS has motor respresentation which could explain certain imitation behaviours particularly those rooted in survival mechanisms. Perception of another animals emotional state and being able to mentalize other peoples behaviour is shown to activate BA9. This gives rise to motor empathy and then this develops into cognitive empathy as we grow and develop. Then, higher cognitive functions come into play (dogs do not develop much past a two years old- The Goldsmith Study on Emotional Contagion was originally designed for young children). So Contagious yawning is really just a functional substrate of empathy. Why is it, that animals yawn when there are no other beings around? Perhaps only its root lies in social signalling, I guess people talk to themselves when no-one is around!

(I IAABC posters are now free with the essential resource guide Essential Training Resource Guide). You will often see a dog yawn in situations such as dog parks, shown below.

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References:

Why do we yawn? University Of Geneva Adrian G. Guggisberga,∗, Johannes Mathis b, Armin Schnider a, Christian W. Hess (Baenninger, 1997; Giganti et al., 2002)

Public Library of Science. (2013, August 7). Dogs yawn more often in response to owners’ yawns than strangers. ScienceDaily. Retrieved March 30, 2015 from www.sciencedaily.com/releases/2013/08/130807204847.htm

American Psychological Association. (2009, August 10). Dogs’ Intelligence On Par With Two-year-old Human, Canine Researcher Says. ScienceDaily. Retrieved March 30, 2015

We would like to thank Olivier Walusinski for his online archive of articles on yawning (http://www.baillement.com)

 

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