Sentience and Emotion in Animal Cognition

1. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press Chapter 13 Emotion “For Charles Darwin, it was obvious beyond any need for argument that non-human animals are sentient ‘… the lower animals, like man’ he wrote in1871, ‘manifestly feel pleasure and pain, happiness and misery’.’ The fact that the lower animals are excited by the same emotions as ourselves is so well established that it will not be necessary to weary the reader by many details’. However, in the belief that identifying problems and finding ways to answer them is a way to move forwards, I shall first emphasize why sentience is still a profound problem, despite the ease with which Darwin spoke about the mental experiences of animals.” Marian Stamp Dawkins, 2006

2. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press Chapter Outline 1.0 Introduction 2.0 Panksepp’s emotional brain system 3.0 The FEAR system 4.0 The SEAKING system 5.0 Summary

3. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 1.0 Introduction The emotion systems of the brain and their interactions with cognitive processing Do you remember where you were on September 11, 2001? You likely do recall that day. And just as likely, you do not recall what you were doing on September 10th, 2001. The events of 9/11 are firmly etched in our brains because of the highly charged emotions that are entwined with the memory of the occurrences of that day.

4. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 1.0 Introduction The triune brain Paul MacLean introduced the ‘triune brain’ concept in1990 to describe the functionally distinct layers of the mammalian brain. It has become a widely-used way of thinking about the overall functional organization of the brain. In MacLean’s view, the brain developed over the course of vertebrate evolution into a three-layered organ, where these layers retain of the separateness of their different evolutionary origins despite being highly interconnected.

5. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 1.0 Introduction The triune brain The oldest layer of the brain is called the reptilian brain, composed of the brainstem -- the structures that dominate in the brains of snakes and lizards. The mammalian brain is layered over the reptilian brain, it consists primarily of a system of brain parts called the limbic system, sometimes referred to as the Papez circuit. The limbic system plays a major role in human emotion.

6. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 1.0 Introduction The triune brain The neocortex or primate brain is the most recent addition to our brain. It consists of a wrinkled covering of the cerebral hemisphere which has mushroomed in primates and humans as compared to other mammals.

7. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 1.0 Introduction Basic emotions and the role of the reflective consciousness Emotional responsiveness is governed by: Classically conditioned responses to stimuli that previously brought pleasure or created pain mediated by subcortical systems and Cognitive appraisals of stimuli in context mediated by the neocortex Neuroscientists have given most attention to the classical conditioning studies conducted with animal models. Almost no attention has been given to the possibility of multiple emotional systems in the brain. Affective neuroscientists have begun to think of mammalian emotion as arising from several separate genetically-determinednetworks of brain areas, each serving an adaptive function.

8. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 2.0 Panksepp’s Emotional Brain System Panksepp (1998) offered a functional definition of an emotional system in the brain, identifying functions ranging from unconditional sensory inputs to emotion control over cognition.

9. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 2.0 Panksepp’s Emotional Brain System Panksepp described a set of 4 fundamental ‘hard-wired’ emotion systems found in mammalian brains: SEEKING forward locomotion, sniffing, investigating FEAR freezing, fright, escape RAGE attack, biting, fighting PANIC agitation, distress vocalization

10. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 2.0 Panksepp’s Emotional Brain System Panksepp described excitatory and inhibitory influences -- such as an excitatory relationship between FEAR and RAGE -- among the 4 systems as well as three other special-purpose systems: LUST, CARE, and PLAY.

11. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 2.0 Panksepp’s Emotional Brain System The feelings of emotion cannot be studied in non-human mammals, although we can make some guesses about the felt experiences of other mammals by observing their behaviors. Emotional feelings can be investigated in humans: a PET study investigated brain responses when subjects self-generated emotions such as happiness, sadness, fear, and anger. They noted different neural maps for the differing emotions both in cortical and subcortical areas. Right panel shows brain areas active for happiness (top) and anger (bottom) (Damasio et al., 2000).

12. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Afferent pathways to the amygdala The FEAR system is a neural system for avoiding pain or injury. The system responds to both unconditional stimuli (loud sounds, sudden movements, painful stimuli, fearful faces) and conditioned stimuli (classically conditioned danger signals, memories).

13. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Afferent pathways to the amygdala Emotion-relevant information arrives at the amygdala via 4 afferent pathways: Olfactory information: from the olfactory cortex Visceral information: from the hypothalamus and septal area Affect-relevant information about internal states: from the hypothalamus, brainstem, orbital cortex, and anterior cingulate cortex Sensory information: from temporal lobe structures

14. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Efferent pathways from the amygdala Efferent pathways from the amygdala mirror the afferent paths, returning signals to subcortical locations and to the brainstem. There are also direct efferent pathways to entorhinal cortex, inferior temporal cortex, and to visual cortex, including the fusiform face area.

15. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Conscious and unconscious fear processing: LeDoux’s Low Road and High Road LeDoux labeled the two sensory input pathways to the amygdala for perception of fearful stimuli the ‘Low Road’ and the ‘High Road’. The Low Road is a fast pathway from sensory receptor to thalamus to the amygdala that bypasses the cortex. It enables rapid, automatic, unconscious reactions to the broad outlines of potentially dangerous stimuli.

16. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Conscious and unconscious fear processing: LeDoux’s Low Road and High Road The longer thalamo-cortico-amygdala ‘High Road’ pathway takes somewhat longer to traverse but allows complex, contextualized processing of stimuli followed by conscious, deliberate responding. The High Road is influenced by social and personal decision making processes and can reflect culture-specific emotional responses.

17. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Fear without awareness: do we need conscious awareness in order to process emotional stimuli? Vuilleumeir and colleagues investigated this question with a patient with right parietal neglect and visual extinction due to damage in his right inferior parietal cortex (see white arrows). If visual stimuli were presented to just one visual field, he had no difficulty perceiving them. However when shown two different stimuli simultaneously in right and left visual fields, he would report not being able to see the stimulus presented to his left visual field -- the ‘neglected’ visual field.

18. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Fear without awareness Unilateral Condition: the patient was able to see the stimuli presented to just the right or just the left visual field 100% of the time.

19. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Fear without awareness Bilateral Condition: the patient reported being unable to see the faces (projected to his left visual field and on to his damaged right cortex) about 65% of the time. The important finding was that fearful faces activated the amygdala whether they were reported as seen or not -- thus without conscious awareness.

20. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press • 3.0 The FEAR System • Cognition-emotion interactions: FEAR • What is the role of the amygdala in cognitive-emotion interactions? • Converging evidence from animal and human studies indicate five areas of cognitive-emotion interactions involving the amgydala: • Implicit emotional learning and memory • Emotional modulation of explicit memory • Emotional influences on perception and attention • Emotion and social behavior • Emotion inhibition and regulation

21. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Emotional modulation of explicit memory Psychological evidence has been available for some time indicating that moderate levels of emotional arousal (most often fear-based arousal) at the time of an event lead to better retention of explicit memories. Pathways include the adrenaline (green) and the cortisol (pink) pathways. Note that both pathways begin in the amygdala, circulate to the adrenal gland, and feedback to the amygdala and hippocampus after passing through the body.

22. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Emotional influences on perception and attention: the Emotional Stroop Test The action of the amygdala can make cortical areas momentarily more receptive to certain adaptively important stimuli. An example of this greater receptivity is found in the Stroop test. Results from Vietnam War veterans show that words that have personal significance (‘bodybag’) are found to gain access to awareness more readily than neutral words, resulting in longer delay in naming their ink color.

23. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Emotion and social behavior Faces -- and eyes -- contain vast amounts of emotionally significant information. The amygdala has been shown to respond to wide-open eyes of fearful and surprised expressions. But what about just the whites of the eyes? A study by Whalen and colleagues (2004) showed that the amygdala was selectively activated in response to subliminally presented fearful vs. happy eye-whites.

24. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 3.0 The FEAR System Emotion inhibition and regulation Fear learning is long lasting and stable, remarkably resistant to change and voluntary control. Research on processes underlying the inhibition of learned fear responses is important, especially for individuals who have experienced traumatic events. Emotional responsiveness can be regulated to some extent by top-down influences from cortex to amygdala.

25. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System Panksepp described the SEEKING system as the appetitive system that makes mammals curious about their world and promotes goal-directed behavior toward a variety of goals objects, such as food, shelter, sex. This concept of the SEEKING system includes classical reward pathways in the brainstem as well as in other subcortical areas.

26. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System In contrast to the FEAR system which gives rise to freezing, hiding, or flight in service of self protection when activated, the SEEKING system is a positively-valenced, energizing system that moves animals out into their environment to forage and experience.

27. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System The primary reward pathways in mammals include the: Mesolimbic dopamine pathway: dopaminergic neurons that originate in the ventral tegmental area (VTA) of the brainstem terminate at the nucleus accumbens in the forebrain Mesocortical dopamine pathway: dopaminergic neurons project from VTA to orbitofrontal cortex VTA is located inside the pons in the midbrain, the nucleus accumbens is located anterior to the amygdala.

28. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System Re-interpreting ‘reward’: from reward to reward prediction to reward prediction error For a long time, the dopamine system was thought to respond at receipt of rewarding stimuli. More recent work has provided evidence that neurons in this system are more responsive to anticipation of reward than receipt of reward.

29. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System Re-interpreting ‘reward’: from reward to reward prediction to reward prediction error An example of an individual dopamine neuron that is inhibited by by a stimulus predicting reward omission: A+: Stimulus A is paired with reward A+ and excites the dopamine neuron AX-: Stimulus A is presented with X with no reward therefore X predicts reward omission X-: When X is presented alone, the dopamine neuron is inhibited

30. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System Reward is more than learning While learning to anticipate a reward is an important aspect of the SEEKING system, other hedonic aspects are also key: liking reactions are neurally modulated by a distributed brain network (shown in green); neural pathways for wanting (shown in yellow) are separable from liking.

31. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System Reward is more than learning Facial expressions for liking reactions are similar in human infants, juvenile orangutans, and adult rat. Disliking reactions are also similar across species.

32. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System ‘Reward pathway’ and drug use All drugs of abuse have their effects on the wanting system via the dopamine pathways and their connections in the midbrain. Natural rewards indirectly affect the reward system by decreasing the action of inhibitory interneurons that normally inhibit the dopaminergic neurons of the VTA, resulting in increased activity in dopaminergic neurons in the VTA.

33. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 4.0 The SEEKING System ‘Reward pathway’ and drug use In contrast, cocaine and amphetamine act directly on the nucleus accumbens to maintain high levels of dopamine at synapses of dopaminergic neurons in the mesolimbic dopamine system.

34. Cognition, Brain and Consciousness: An Introduction to Cognitive Neuroscience Edited by Bernard J. Baars and Nicole M. Gage 2007 Academic Press 5.0 Summary Mammals have separate emotional systems in the brain, each with patterned, innate responses to stimuli in the expected environment of the species related to survival. Systems such as the FEAR system and the SEAKING system have both conditioned and unconditioned responses to stimuli supported by separate neural networks: FEAR relies on the amygdala and its connections, SEAKING relies heavily on the mesolimbic and mesocortical pathways of the VTA. Each of these systems can come under cognitive control and reciprocally influence higher decision-making, appraisal systems, and consciousness. Each system is capable of elaborating distinctly different subjective feelings.