Neuroscience Of Licking & Sender-Receiver Mechanisms. Are They Conflict Reducing, Disengagement Markers, Arousal Or Congruence Signals?

Why do animals, particularly canines, lick their lips? Is it a sender-receiver dance, a physiological response to changes in internal environment, a reciprocity sign or a signal of some kind of deceit?

We take a look at this phenomenon from a number of (neuroscience, physiology, behaviour, psychological, medical, ethological and philosophical) perspectives. How an animal signals externally to reflect changes to his internal environment and how that is reflected in his body language raises many questions and it would seem, is a subject which requires some more understanding.

The Vagus Nerve:
Anyone who watched our Neuroscience Of Behaviour Seminar would be familiar with the Vagus Nerve. Just to recap, This is Cranial Nerve 10 (or X) CNX or VN for short.

This is the beginner seminar (which is all explained in very easy terms and a good refresher for you science degree people who might have forgotten some of the terminology. Also, epigenetics is explained and how it all fits into place with behaviour)
http://www.simplybehaviour.com/course/science-of-behaviour-beginner-seminar/
This is the next one along which weighs up all of the current evidence, neurotransmitters, hormones, brain anatomy etc..
Introduction To the Neuroscience of Behaviour On-line Seminar (Degree level)

In the nervous system this nerve travels to the heart and gastric regions and is responsible for the parasympathetic nervous system response. It is absolutely fascinating because this nerve has predominantly afferent nerves which transmit information back to the central nervous system (CNS) as to the state of the bodies organs. This is the basis of what is commonly described as the “gut instinct”. These gut vagal afferent’s modulate anxiety and learned fear (2014 Journal of Neuroscience). Between 80 & 90% of the VN’s afferents communicate to your brain about the state of your viscera.

These are emotional feelings, they modulate mood, fear and anxiety. These signals travel down to your organs signalling to them that they can be in a state of rest (where you can digest) or, fight-or-flight (in the face of danger). Research has shown that if you cut the afferent nerve fibers and set animals up with a series of learned and conditioned fear situations, found that when the communication between the VN and the brain was interrupted, there was less fear. When the two way system was cut, rats still retained learned fear responses, but a much lower level of innate fear.

So, healthy VN communication helps you keep the brakes your nervous system by helping you to use neurotransmitters such Acetylcholine and GABA. They lower the heart rate & blood pressure and help you to digest. So, we hope you can see that the VN plays a huge role in how an animal is responding to fearful situations. With this in mind, can you now see how the phrase “sick to the stomach” comes in?  One of the first signs of nausea, or an uneasy feeling, will be the gut response to a situation. This is making the animal feel physically uncomfortable. The effects of tension reduce saliva flow and the mouth becomes dry. This is why you will often see animals licking their lips with increased frequency in uncomfortable situations.

vagus-nerve

 

 

Image: Courtesy of Bloomsbury Educational Ltd

Nausea
Has the function of aversion and avoidance. The vagus nerve sends neurotransmitter impulses to the smooth muscle of the stomach that result in contraction and forward propulsion of gastric contents (normally) and controls the motor (muscle) response of the intestine. The neural pathways, sensation of aversion and avoidance are common to dogs, cats, ferrets and humans. Dogs are able to experience the same unpleasant sensation as humans.

Studies have shown that we can condition animals to avoid substances that have been paired with or caused a nausea type response. Nausea (according to the Boyd Group’s report) is even more aversive than pain. The sensory component of nausea is very difficult to measure. Could it be, that our animals feel nausea in these uncomfortable situations? Nausea can be induced by the same stimuli as vomiting but at a lower threshold. The sensation of nausea involves higher brain centres too! Receptors carry information by the VN from the abdomen and the area in the medulla of the brain which is involved in detecting chemicals and hormones in the blood.

The neurotransmitters involved in controlling nausea and vomiting are Dopamine, Histamine, 5HT & Acetylecholine. The opiod receptors are also present. The higher brain inputs are involved in more anticipatory behaviour. Such as, a fearful sight or a repulsive smell. The Nucleus Tractus Solitarius (NTS) in the dorsal brain stem integrates information and coordinates any autonomic motor outputs such as panting, sweating tachycardia. Gastric rhythm increases, then the sensation of nausea and if the feedback slows down the gastric rhythm, the nausea subsides.

The clinical manifestation of nausea in dogs and other animals is characterised by excess salivation, lack of appetite, licking of lips, increase frequency of swallowing and depression. Often, a reliable indicator of stress in dogs (particularly those that are real foodies) is them not wanting to take treats. Vultures are reported to use vomit to dispel any potential threats and make them lighter so that they an flee quickly. Other animals (including humans) use vomiting as a defense against harmful chemicals (such as in morning sickness). Could it be, that the nausea is a way of your body picking up on signals of harm that do not necessarily amount to actual vomiting?

functional-organization-of-peripheral-nervous-system

 

Image: Source unknown

Ekman reported that the tongue is often used to show that the animal is pensive, or trying to come to some kind of decision. Sanberg (University of South Florida) proposes “what is at issue, is the brain’s ability to learn that it has discovered the right approach to a challenge”
Could it be, that lip licking serves some kind of problem solving mechanism in dogs? In order to be able to test this, we would need to measure activity in the anterior cingulate cortex which is the region of the brain associated with emotions and decision making. This area is activated during anticipation of what could happen next. Could this be part of why we are observing it, as some kind of “cut of signal”? Could this be an innate mechanism, which serves to buy us more time, to figure out what to do? Then, if it works, it becomes a problem solving tool. By solving these problems, the behaviour itself becomes somehow reinforcing.

When Licking Is A Problem:
Joydeed Bhattacharya (College Of London) looked at brain rhythms when people were trying to solve verbal problems. It was clear that we can become mentally blocked when there is an excessive amount of gamma brain rhythm. Lick granuloma, which often results in a very nasty sore on the dogs anatomy, appears to be psychological in its origin. It is related to stress, anxiety, separation anxiety, boredom or compulsive behaviour patterns. They are prevalent in dogs that are often left alone for long periods of time. The act of licking releases endorphins (your body’s own little morphine system), this reduces pain and makes the dog feel euphoric. This means that the licking in itself, provides positive feedback and then an addiction to the act of this behaviour. Sometimes animals in captivity will develop what is often termed vacuum or sterotypical behaviours. These can involve licking walls, bars etc.

DNA evidence suggests that flank sucking and a form of autism in some breeds are related. There is a genetic pre-disposition for this type of behaviour and it is only is expressed when the animal is under stress, conflict, frustration, maternal separation, lack of stimulation, exercise or enrichment. There have been suggestions of a dietary component (Vit B6 & C) too and a research study showed that this behaviour decreased when supplements were given. Also, the presence of another dog has shown to reduce the behaviour, (rather than them living alone).

We have developed a series of survival guides to train your dog using enrichment, clicker, positive reinforcement and to set your dog up to succeed in a variety of settings, giving your dog the right start will drastically reduce the risk of stress behaviours.

For the slightly more science based background we cover all of the latest neuroscience findings relating to behaviour. Check out our 2 on-line seminars on the introduction to the neuroscience of behaviour:

 

Also, The Essential Dog Trainers Resource Guide (posters, handouts, habituation schedules, socialisation, aggression ladder, critical periods, learn that you return protocols, information hand-outs etc):
Essential Training Resource Guide

Example posters:

As you can see, the brain and nervous system work together providing us with sensory and motor outputs that have some function for the animal. This behaviour can sometimes remain even when the function of the behaviour has long lost its benefit. So, if these behaviours start to happen outside of their original context and have some degree of dyscontrol in the way they are initiated or terminated, they are likely to fall under the umbrella of obsessive compulsive.

When animals develop licking behaviour, they tend to focus on a particular area. It is possible that this has some form of medical origin. Excessive licking could be due to pain, inflammation infection etc and stress will contribute to this. Then it starts to fall within the realms of a neurologic disorder, long after the medical condition has cleared. This then becomes a learned behaviour and leads to an increase in neurotransmitters, receptors and the response that the owners give through inadvertently reinforcing through stress (punishment) or reward (getting attention) in some way.  Gary Landsberg (North Toronto Vet behaviour specialist- Canada) states that sucking, pica, smacking lips, gulping & licking could also be a medical neurological, gastrointestinal or behavioural origin.

This is particularly observed in animals who have a degree of frustration or conflict relating to their environment. Also, maternal deprivation can play a major factor and stereotypical behaviour is often induced from an inability to cope & some kind of CNS dysfunction. Even though it starts out as a mechanism to help the animal cope there is a higher level of activity in the striatal dopaminergic system, there is a change in the serotonin pathway, the frontal, pre-frontal cortex and the amygdala, plus a genetic and breed component.

Licking is derived from a normal behaviour (perhaps a missing maternal behaviour, which is essential for helping to turn on the genes that help an animal cope with stress, such as the gluco-corticoid system). The increase in drive for this behaviour, comes from an approach-withdrawal conflict behaviour. Conflict because they are motivated to perform two opposing behaviours and this is why, this type of self trauma occurs. For example if an animal wants to greet, but is prevented or restricted from doing so.

These types of displacement behaviours occur when there is conflict, arousal, frustration or lacking of enrichment. A Brazilian research study looked at 20 dogs with ALD (acrial lick dermatitis), it was found that they had serious anxiety, were never played with and 70% were not walked!

Gustation/Olfaction:

Animals use their tongues to enhance sense of smell. When they lick a surface or extend their tongues, they transfer molecules via the tongue to olfactory receptors and then to the vomeronasal organ. Keeping his nose wet is essential for him to be able to lower the surface tension of the scent molecules so that they can be effectively translated to give him the required information from his environment. Dogs have about 250 million smell receptors and a highly developed sense of smell. It is even reported that they can detect a single molecule of vinegar in a swimming pool. If the function of licking his nose is to gather information about a novel aspects to his environment then could it be that this behaviour serves to help him gain essential information from his environment, like some kind of olfactory detection mechanism? We know that dogs can detect very small chemical changes in humans (such as alert dogs for diabetes, or epilepsy), it would be plausible to assume that licking of the nose gives accurate readings about chemicals in the environment, such as stress secretions, pheromones etc.

scent receptors

 

Image: Boones Creek Beagles

Licking Lips In Hunger/desire:
Some animals lick objects to obtain mineral nutrients, dogs lick to obtain water. Reward systems are activated by the sense cues. Anything that is desired will stimulate the same pathways and neural regions and it is the same for food. Any positive reinforcement trainer will know this already. The brain areas involved are the striatum, amygdala and of course the hypothalamus. Hunger and satiety centres are focused around the ventral medial hypothalamus and when these areas are activated in response to items that are wanted, or desired, the signals in the reward centre interpret them as being important for survival. Evidence shows (in humans) that luxury items like expensive cars, activate the mesolimbic dopamine reward system, these are secondary (learned) reinforcer’s and the same mechanism comes into play with food and drugs. So what? Well, the physical response to this state of reward includes the secretion of saliva, triggered by the sympathetic and parasympathetic nervous system. The gustatory system is neurally regulated, stimulation of the metabolic pathways prepare the body to consume, so that mastication and digestion can occur. This is a by product of the autonomic system being stimulated via the hypothalamus and salivation happens to signal any desired stimulus. This would increase licking of lips in anticipation of the reward!

Drooling:
Remember that anxiety activates the fight or flight system in the body, and that means that some of the functions in your body are activated, while others shut down. So it’s possible that salivary glands are activated, or that some part of your body that controls salivation is shut down. The frequency of licking might be less in this situation and the animal can appear shut down.

Solicitation (sometimes wrongly called submissive licking):
Mothers typically lick their offspring clean immediately after birth. This is necessary for many reasons. It frees the offspring from the amniotic sac, cleans, dries, stimulates breathing, digestion and from an epigenetic perspective, it actually turns on gene production systems, particularly those associated with the glucocorticoid system. Studies show that young who have attentive mothers (measured by the amount of licking towards their offspring) have a much higher resistance to stressful situations because of the activation of these genes (evidence of epigenetics). Licking other animals mouths is often observed in greetings, old and new. This correlates well with Dolco’s research, which noted a positive initial interaction with a new friend gives the relationship a boost and helps to attenuate any negative outcomes. Sanberg talks about the social cognition network in response to approach avoidance conditions. By licking other dogs, it gives a positive evaluation of the approach behaviour and the positive impact of the interaction actually increases sensitivity in the amygdala and superior temporal sulcus. When they looked at the impact of hand shaking between two humans greeting for the first time, they found there was greater activity in the nucleus accumbens compared with those that did not shake hands.. This indicates a positive emotional experience. Perhaps licking another dogs face is a way of evaluating a social interaction, and is nothing to do with the popular “dominance-submissive” explanation (which is highly outdated).

Grooming:
Licking is a common way for animals to keep themselves clean. Cleaning and taking care of yourself and each group member actually increases oxytocin levels and has the added benefit of helping to untangle fur. It could be a self soothing behaviour, or a displacement type response, that serves the animal more time to think and assess the situation for risk (as in the Ekman’s research).

Communication/”Calming Signal”:
According to the experiment by Gazzano (2010) Mariti (2010) & Mariti (2014), where they observed dog-dog encounters in various standardised contexts (such as familiar, unfamiliar, female familiar, male unfamiliar-dogs) off-leash, and in a fenced area, for a period of 5 minutes.

They observed over 3,000 behaviours and analyzed the 21 signals (which were originally described by Rugaas), such as looking away, turning head, play bow etc. The ones that involve the mouth and licking (what we are discussing here) were “licking nose” & “licking the other dogs mouth”. The conclusion of this study was that interaction was the main factor when these types of behaviours were displayed and when so, there was a decrease in chance of aggression (significantly).

They concluded that licking lips and other licking behaviours (and other calming signals) do play some form of communication role and appear to have some impact on the behaviour of the other party. Whether the dog instinctively knows this is going to happen, he has learnt it, or he is merely signalling some kind of internal discomfort. It would appear his lip licking has an external representation of  mild arousal and has some function to calm himself down (and the other party being calm as a by product or learned behaviour) The fact that the other dog does not aggress him because of this, is another factor, it seems to work.

It is a quiet signal, less expensive and it is possible that the response he gains from doing this and it being part of the arrangement is the factor that maintains its use. It works around other dogs when there is mild discomfort, which could imply that it is a conditioned behaviour which has communication and physiological mechanisms. Behaviourally, calming another animal down because your body language is indicating your are no threat is quite an advanced thought process. Does this imply capability of deceit, because if you set out to have an affect on anothers behaviour for your own gain (even when the expense of that gain does not really benefit you to any great lengths) it implies empathy, understanding and to be able to de-centre from your own cognition i.e. how your behaviour directly affects another. If this is the case we need to work out if mirror neurons (which are responsible for your brain’s perceptions of what another is doing and believed to be part of the empathy system), are activated in these contexts. So, Greg Berns, yet another reason to get your FMRI gear on and do another wonderful experiment to help us understand more.

If we identify the brain regions activated we can very easily see what type of behaviour response aligns with which brain region activation. .. Is lip licking just a physiological response to a situation which makes your nervous system respond and licking lips helps the dog to calm down and then the by product of this, is that the other dog sees a non-threatening display (some body language could just afford that receiver interpretation by its very nature) Or does the lip licker know what he is saying?

It is likely that this can be learned in socialisation, which is why it is important to help your dog have great interactions with many other dogs (people and settings).  Physiologically it certainly seems to signal some low level of arousal. This means that we need to take notice of these low level signals. If they are ignored they have the potential to escalate. This is the take home message for any person who owns, interacts or is involved with dogs. One of the main findings of the Simona Cafazzo study, (which looked at stress indicators in body language such as lip licking, pacing and measured physiological markers) was that animals who get exercised and the opportunity to socialise were far more relaxed. The exercise impact was greater than any of the other variables (such as cage size etc)

Communication (and the ability to deceive)
Yes! Picture this, me, cuddled up on the sofa with my little puppy. Along comes grown up dog, (beware owner interpretation coming up) spots the lack of cuddles, he is not getting. Works out a strategy to get up and get to the cuddle spot (next to me). Next thing, he offers a play bow and a full ninja circle to reveal his bottom (one of the best invites to play- ever. He is saying “look, my harmless end, I really want to play with you”- to the puppy) Puppy cannot resist, she jumps down and starts boxing him with her paws. Older dog disengages, jumps up and snuggles right up next to me and just sits looking at her. Puppy looks a bit miffed but the older dog is content- he has won! Despite the anthropomorphism of this observation, the older dog has employed some form of deceit to achieve his goal and that requires spatial and cognitive planning. He set out to deceive!
A study using primates in a zoo to test deceit, showed that they were willing to hide bananas and rocks (the rocks were to throw at visitors- do not go to that zoo!!) and they showed that animals do actually set out in some way to deceive another, particularly when it comes to resources. Studies show that deceit is, in-itself, self-reinforcing.

We know a dog has the cognitive capability to deceive in some contexts, so if he is able understand how to use his body to deceive another, then it would be logical to assume that when he licks his lips in certain contexts he is trying to convey a message and it is likely that he is aware of the affect that will message will have on the receiver. Does that make sense? Whether he would use this particular behaviour to deceive is another question. One might guess that if it has the desired outcome, it could be employed to help him get out of all manner of sticky situations. Its certainly going not going to escalate them 🙂

It is likely that your dog is anxious or fearful if you notice combinations of the anxiety and/or fear behavioural signs, such as licking lips, with ears back, and a tense facial expression. Combinations of signs vary between dogs and in the same dog. Also, physical differences in some breeds, mean it can be harder to notice behavioural signs in some dogs. Even if you only notice one of the behavioural signs, this can still be a good indicator.

Bristol University have put together this information to help educate people on dog body language and the behavioural signals of anxiety and fear:

behaviouralsignstable

It is general consensus, that if you see an increase in frequency of these behaviour signs, and along with this you see repeated lip licking and or,  an increase in any of the the other signs in specific contexts (and not in other situations), it is likely that he is communicating some degree of discomfort in these environments. Be particularly mindful of him panting, salivating, yawning and obviously licking his lips (out of context for a physical reason, such as exercise, heat, presence of food).

The research indicates, that whatever the sender-receiver (physiological, neurological) basis there is for this behaviour (with respect to lip licking and any of the other “appeasement”, “calming”, “cut-off” type behaviour), they are a communication. People need to be mindful of context and positively help an animal to disengage and get to safety. He will definitely thank you for listening to him and it will prevent his behaviour escalating up to this (part of the essential guide as shown in slideshow above):

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Or you can purchase it here:
Essential Training Resource Guide

Beerda et al measured hormonal, neurotransmitter and immunological levels to represent manifestation’s  of chronic stress in various spatial housing scenarios. One of the behaviours associated with the stress response is lip licking. They found that when dogs were spatially restricted preceding (the control) the bad weather condition this induced early stress which was reflected by increased salivary and urinary cortisol, less responsive HPA to sound blast, (exogenous CRH- induced ACTH, cortisol and lymphocyte proliferation). The bad weather (control) followed by restriction give a negative appraisal in the reduction of space, spatial and social restriction and this was attributed to their stress responses.

Interestingly, Male and female dogs differ in that bitches seem more susceptible to acute stress and housing stress (as is shown in their HPA response to sound blast and exogenous CRH). The conclusion of this study was that the preceding period of circumstances greatly affected the magnitude of the behavioural and physiological response to stress. The salivary and urinary cortisol measurements seem appropriate for assessing chronic stress and poor welfare. The urinary catecholamine, lymphocyte proliferation and peripheral leleukocyte measurements require further comprehension.

Signals such as lip-licking seem likely to carry information. It could be argued as to whether or not information is the sort of thing that can really be carried or contained?  Critics of animal and human information based communication, such as Scott-Phillips, Kirby, Rendall, Owren, and Morton, find that, the “state” of the signal has an affect on the probabilities of the various environmental contexts (we often see this behaviour paired with other environmental cues).  In order for a receiver to adjust his behaviour with the context, the signal should be associated and not independent of it.  Which is why is it important for us to understand that context is an important factor when considering if a dog is licking his lips because he is hungry, or if he has, a low head, ears flat and is visibly unable to escape (an all to familiar site when we see a child hugging a dog). The picture below is a classic example of the type of behaviour you might see, that would precede a dog “biting out of nowhere”. Almost never, does a bite come out of nowhere.

child hugging dog

Is the assumption, that information is a useful a way to understand animal communication (According to Peter Godfrey-Smith)? What about co-operation?  It would seem that information and influence seem to come as a package deal. Perhaps our explanation of signalling needs a more detailed view than one of cooperation and reduction of potential conflict? The Ladder of aggression (see above) gives some scale to this.

The sender-receiver systems seem to work in some way to tie information together. Does the way the receiver acts have consquences for both side? Do they have common interests? Or, do they just decide which act is better or worse. Any deviation from these behaviours would not make either party better off (Nash equilibrium). Philosophers state, that if a specific signal is given, it helps the receiver to produce an act that is “in tune” with that signal. This is some form of postural congruence or congruent feedback which naturally matches or mirrors the senders signal in some way (thinking from a neuroscience perspective, we get back to empathy and mirror neurons- do canines have these?) Please read the article on yawning for further explanations and evidence:

Why Do Dogs Yawn? The Neuroscience Of Empathy

If you want to understand more about empathy in dogs, we have put together a short 7 day intensive course which covers all of the current research into the neural mechanisms of emotional contagion and empathy. Please go to: Emotional Contagion & Empathy Course

Signals are complementary, which demonstrate some form of common interest, if the basis of these signals is biological (in terms of reflecting some internal changes) then it is likely, that through some genetic or learned process the very nature of these signals affords the receiver response.

Partial common interest between dogs makes this signals worth sending. By not reading (as humans tend to, with the best intentions sometimes) the sender information, the animal will feel internal conflict (approach avoidance causing stress) and there lies the problem. When communication is ignored (or not received), that is when you seek alternatives (see ladder of aggression). That is the last thing we want. It is expensive, stressful, unnecessary and actually HIGHLY effective- as in, a bite will always move a hand away!

By observing the subtle signal changes in contexts, your animal is sending information, which if not received will degrade. The messages he sends are physiologically limiting/inexpensive (he cannot talk) but they have the intention of complete, or at least partial, common interest (to reduce discomfort). In the case of lip licking that interest, is not one of conflict.

Crawford & Sobel (1982) Informative signaling is viable “to the extent” that there is common interest, but it may be a good sketch. The sketch can be filled out by looking for different ways in which partially informative signalling can be maintained through partial common interest.

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References:

Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses.
Beerda B1, Schilder MB, Bernadina W, van Hooff JA, de Vries HW, Mol JA.
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Herrstedt J (2009). Antiemetics: an update and the MASCC guidelines applied in clinical practice, Nature Clinical Practice Oncology 157: 865-880.
Qin X Y, Pilot M A, Thompson H and Scott M (1993). Effects of cholinoceptor and 5-HT3 receptor antagonism on erythromycin-induced canine intestinal motility disruption and emesis, 108(1): 44-49.