It may be surprising, perhaps shocking for most people to realise that the generally accepted consensus among neuroscientists working with human and/or non-human subjects is that only humans are conscious (Panksepp, 2005a) - the term consciousness as used here refers to the ability to experience internal, personal subjective experiences (AFFECTS is the psychological term for these for which Panksepp has coined the term affective neuroscience) such as sadness, joy, happiness, fear, anger, etc..
This has not always been the case, throughout the 19th Century many scientists readily accepted the concept of the mind, emotions and feelings as psychological phenomena. It was the 20th Century, with the dawn of the ‘hard’ behavioural scientist movement, spearheaded by behavioural psychologists like Watson, who considered any kind of mind/mental/cognitive states as irrelevant, unscientific clutter.
Instead they concentrated on stimulus – response behaviours that could be measured (see McMillan & Rollin, 2001, Greenspan & Baars, 2005, Lecas, 2006 for reviews).
Over the last 25 years, neuroscientists have contributed a vast amount of information on emotional learning, and Joseph LeDoux (1996) on the neurophysiology of fear in particular.
The question arises as to whether non-human animals EXPERIENCE fear, that is, do they have the same aversive internal mental FEELINGS as humans that accompany the obvious behavioural response, such as a dog fearful of thunder?
The answer to this question, according to Jaak Panksepp is...
“…even in well-funded areas such as fear conditioning, there is scarcely an investigator who dares explicitly address the ever present worry—do animals experience fear?...” and “…fear of being tarred with the brush of anthropomorphism…” (Panksepp, 2005a).
Panksepp goes on to explain one reason for this...
“…Joseph LeDoux, the best funded animal emotional–memory researcher in America, publicly related how he failed to obtain approval for his initial grant applications until he extracted the term “emotion” from his proposed work to study classical-conditioning of fear and replaced it with learning and memory terms…” “…Other neuroscientists interested in emotions had comparable, but more sustained, funding problems throughout the last quarter century…” (Panksepp, 2005b).
Panksepp argues that rather than being a recent development of the human neo-cortex, the roots of consciousness (he uses the term AFFECTIVE CONSCIOUSNESS to reflect its internal, FEELING nature) can be traced right back to early mammals in deep ancient sub-neocortical limbic regions of the brain.
Panksepp and his colleagues have identified seven basic emotional systems (capitalisation of the names indicates that they refer to specific brain neural systems that are only partly understood):
SEEKING, RAGE, FEAR, LUST, CARE, PANIC and PLAY (Panksepp 2005a, 2005b). The human neocortex in all its cognitive complexity further processes these primary affects into more elaborate emotions such as love, shame and empathy (see Table 1). The evidence for these core emotional systems is laid out in detail elsewhere (Panksepp, 2003, 2005b, Watt, 2005), but here is a summary:
Opiate and dopamine agonists are drugs of abuse in humans and also attractive to other mammals.
PET studies show remarkable similarities in basic emotions in humans and other mammals and these emotions arise in deep, subcortical areas of the brain (see Fig. 1 and Table 2).
The anatomy and neurochemistry of these subcortical areas is remarkably similar in all mammals and it is clearly evolutionarily homologous.
Areas of the brain that evoke consistent behavioural indicators of positive and negative affective states in humans and animals when electrically stimulated are remarkably similar and the most powerful ‘feelings’ are generated in deep, subcortical areas.
Evolutionary common sense suggests that emotion is an evolutionary extension of homeostasis, and that cognition is an extension of emotion and the mammalian brain has evolved to seamlessly integrate these three levels as HOMEOSTASIS – EMOTION – COGNITION (Watt, 2005). The homeostatic mechanisms are largely unconscious, but these evolved into conscious, emotional feedback systems to let the animal know how things were going (well, or badly). It is likely that affects, or feelings are the only true reinforcers, a view in contrast to the behaviouristic assertion that outside events can reinforce behaviour with no associated feeling (see Watt, 2005 for full discussion).
The SEEKING System
Coppinger & Coppinger (2001) describe in great detail the evolved motor patterns in various types of dog - livestock guardians, headers, heelers, hounds, pointers and retrievers. When a Border Collie is in eye-stalk (see Fig. 2), is this just a behavioural motor pattern, or does he FEEL some pleasure as well? The answer to this question is an unequivocal YES, and his feeling arises in the same dopamine-driven SEEKING system that gives us pleasurable feelings when we’re engaged in a task we enjoy.
This same system is the powerhouse behind extreme pleasure-seeking activities such as drug abuse and even addiction to extreme sports (Franklin, Zijlstra & Muris, 2006). In animals the genesis of many ‘behaviour problems’ is the lack of opportunity to perform strong, innate behaviours and so adopts other, inappropriate behaviours instead. Some initially fear-related aggression problems in dogs turn in to ‘addictive’, dopamine-driven pleasure-seeking behaviours not unlike humans who enjoy the exhilaration of ‘escape’, as their nucleus accumbens is flooded with dopamine after terrifying them selves by jumping off a tall building (B.A.S.E. jumping).
The FEAR System
Although there are species differences in how the Fight-Flight-Freeze system is engaged when an animal is aroused by a novel and potentially dangerous stimulus, the underlying mechanism is the same in all mammals as mapped out by LeDoux, 1996. Information about external stimuli is relayed by the sensory organs (ear, eye) to the thalamus. A signal from a sudden noise, for example (see Fig. 3), arrives at the auditory thalamus that relays the data on to the sensory auditory cortex (High Road). The sensory cortex has the benefit of advanced cognitive processing and can therefore evaluate the incoming data, make a risk-benefit analysis of all the possible reactions and choose the best fit before sending the data on to the amygdala for an appropriate emotional response. The sensory cortex’s job is to prevent an inappropriate response rather than to produce an appropriate one.
There is also a smaller, faster neural pathway running from the thalamus directly to the amygdala (Low Road), that is the storehouse for emotionally charged memories. The Low Road route cannot make fine distinctions, it has an important advantage over the High Road route – speed. In an emergency this rapid response could be a matter of life or death. LeDoux calls it The Difference Between The Quick and the Dead.
Panksepp (2005b, 2006) has identified another route, the “Royal Road” that runs between the amygdala and the periaqueductal gray (PAG) of the midbrain, and it is this system that constitutes the core FEAR system. It is here that the obnoxious and aversive FEELINGS of fear are generated and help an animal to anticipate and avoid danger. Other neuroscientists have largely ignored this system as meaningless output of little importance in the study of anxiety.
However, Panksepp argues that it is central to understanding anxiety disorders, pointing out that this FEAR system is unconditional in that it generates these ‘bad feelings’ simply by electrically stimulating it. It is also involved with the freezing and flight response and anxiolytic drugs ameliorate anxiety by modulating this FEAR system. Some dogs with a long-standing fear of thunder can become withdrawn, ‘depressed’ and jumpy and it is the FEAR system that is responsible for these states.
The RAGE System
The RAGE system does just what it says on the box. In adults it is modulated by higher cognitive centres whereas children are less inhibited and therefore fly into tantrums easily.
Other mammals also show rage and the emotion can be elicited by direct brain stimulation.
The LUST System
We talk in terms of instinct when referring to reproduction in other mammals, but the highly subjective erotic FEELINGS associated with it arise from ancient and deep subcortical structures common to all mammals.
It is therefore reasonable to assume that the purpose of these highly desirable FEELINGS is to ensure the propagation of the species (Panksepp, 2006).
The CARE System
The behaviour of a whelping bitch to the distress calls of a separated puppy is a wonderful example of the CARE system. After the last pup is born, and for a duration of about thirteen days, the bitch is primed to respond to the distress calls of any puppy that wanders away from the nest (Coppinger & Coppinger, 2001, page 217-220). The CARE system (see Fig. 4) is present in all mammals (birds too) and triggered by the changing levels of oestrogen, progesterone, prolactin and oxytocin, gives the mother the innate ability to care for her young (Panksepp, 2006).
The PANIC System
Separation related disorders (SRD) are common behaviour ‘problems’ in dogs, but how often do we relate how a whimpering dog FEELS when left alone to how we feel when, for example, we lose a loved one? Throughout the ages poets and philosophers have expressed love lost and the loss of meaningful social bonds in painful metaphors - broken hearts, hurt feelings - and this is common across many diverse cultures including Western and the Middle and Far East (MacDonald & Leary, 2005).
Eisenberger and Lieberman (2004) have shown in fMRI studies that physical pain and social pain share common cognitive and neural systems in the brain and suggest that this is an evolutionarily adaptive setup that helps to ensure that conspecifics do not become separated from each other and vulnerable to danger, and in young, dependant mammals in particular, this system is essential for their survival.
Panksepp and colleagues have carried out extensive research over the last 25 years on separation distress in non-human animals (see Panksepp, 2003, 2005b, 2006 for summaries) and have also found considerable overlap in the brain areas for physical and social pain. They also found that opioid analgesics were very effective at alleviating the cries of separation distress in dogs, guinea pigs, rats, primates and even chicks, and that human sadness and guinea pig separation distress share remarkably similar brain regions (see Fig. 5) (Panksepp, 2003). In addition to opioids, neuropeptides such as prolactin and oxytocin also powerfully ameliorate separation distress and the feelings of depression and these substances open the door to the possibility of new and exciting pharmacologicals for treating such emotional states in the future.
The anatomical and experimental data is irrefutable that the sub-cortical areas of the brain that generate and regulate both physical and social pain are evolutionarily ancient and are shared by all mammals. The ethological fact that gentle handling of the very young can stop their cries of separation, in part through the release of endorphins and oxytocin, and if left alone can suffer catastrophic ‘psychic pain’ and will often die (Panksepp, 2005b).
All of this has profound implications on those dealing with animals on a day-to-day basis, such as the veterinary and allied professions. Should veterinarians perhaps be considering the use of the longer acting opioids such buprenorphine, even fentanyl patches or morphine infusions, not just for their analgesic effects, but also for their powerful antidepressive effects on patients separated from their owners for any length of time?
The PLAY System
We probably all take for granted rough and tumble play in pets (see Fig. 6), but the apparatus for play, the PLAY system, is actually built right into the brain (Panksepp, 2005b). Play is common across all mammals, but in ethological terms it is very expensive, even dangerous. It must therefore have a useful biological function where the benefits out-weigh the risks. Traditionally, biologists and ethologists believe that the purpose of play is to give animals safe opportunities to practice hunting and mating skills. But there is rather more to the PLAY system than this.
Scientists have tended to lump play activities in with seeking activities and treat them as different facets of the same thing. But this is incorrect. The PLAY system and the SEEKING system are separate systems and work through different neural networks. When we see animals engaging in PLAY, they’ll often engage some of the predatory behaviours we associate with the SEEKING system, for example 'stalking' each other, 'attacking' and 'biting' each other and so on, but this is simply because they have a limited behavioural repertoire. What you’ll notice is that dogs use different chains of behaviour in PLAY than they do in SEEKING – play bows, high-pitch barking, tug of war games on a toy for example.
The PLAY system and the SEEKING system are often antagonistic to each other rather than synergistic and cannot be engaged at the same time. A good example of this is the routine use of amphetamines (Ritalin) to treat children with Attention Deficit Hyperactivity Disorder (ADHD). Amphetamines work through the SEEKING system and increase attention and exploratory behaviour by increasing the availability of dopamine in the reinforcement circuits of the brain. In 'normal' people psycho-stimulants like amphetamines increase arousal and activity levels. If you’ve ever taken Speed, you’ll remember the effect of racing thoughts and chattiness, the inability to keep still to the point of agitation and the inability to sleep. Remarkably similar to some of the hyperactivity signs seen in kids with true ADHD!! But if you give these kids psycho-stimulants they have the opposite effect and calms them down! The reason for this paradox remained a mystery for a long time, but we now know that ADHD is a disorder of an over-active PLAY system and has nothing to do with arousal and the SEEKING system. Stimulating the SEEKING system in these kids antagonises and suppresses the PLAY system. Panksepp touches on the possibility of utilising rough and tumble play as part of a management program for children with ADHD, rather than just relying on amphetamines, that suppress the urge to play (Panksepp, 2006).
The opioids (natural endorphins in the brain) play a major role in the PLAY system and the role of dopamine is insignificant by comparison (compare this with the SEEKING system, where dopamine is the major player). When animals play, there’s a lot of body contact which causes the release of endorphins (and other neurotrophic substances, call them 'brain food' if you like) in the brain that makes them feel good – euphoric. And because the animal is relaxed, unthreatened and therefore un-aroused, the PLAY system is engaged facilitating the growth of neural circuits that strengthen social attachments and ‘getting along with mates’. The PLAY system is not engaged when the animal is aroused. If the nature of this arousal is aversive, that is the animal feels threatened, then the FEAR system is engaged. On the other hand, if the nature of this arousal is appetitive, then the SEEKING system is engaged instead.
One intriguing, and highly controversial possibility is that laughter and joy may not be unique to humans and many mammals have a marvellous sense of fun (Panksepp, 2005c) and this poses an interesting question: “could your pet have a rudimentary sense of humour?” (see Fig. 7).
Other evidence supporting these claims (Panksepp, 2005b) include: (1) amphetamines stimulation of the nucleus accumbens (the area of the brain flooded with dopamine at times of intense pleasure and mirth in humans) induces the same vigorous 50kHz chirping in rats when they are tickled, (2) rats that have been tickled become very friendly toward the tickler and chirp at 50kHz as he/she approaches the cage, and (3) these rats consistently choose to stay close to other rats that chirp a lot rather than those that do not.
In this summary we have made only a tiny scratch on the outer mantle of the massive volume of data now available on the rich mental lives of non-human animals, and we appeal to everyone responsible for the wellbeing of pets and other animals to take the time to explore this fascinating body of work and take advantage of it in their everyday endeavours to promote a better understanding of both the positive and negative impact we humans have on the animals in our care.
Jaak Panksepp’s book, "Affective neuroscience: the foundations of human and animal emotions" (Oxford University Press, 2004, ISBN: 019517805X) is the definitive summary of the evidence for the seven core emotional systems discussed in this brief article. Watt (2005) says about this book:-
“I’m reasonably confident that future neuroscience students will look on this textbook as one of the seminal publications on the subject of emotion and the brain…”
How does the dog in this video feel as she tries to find her ball in the long grass?
What is going through her mind as she searches?
Can she use her memory like we humans can and try to recall the last time she remembers having the ball in her mouth?
Is she thinking anything at all?
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