Cognitive Neuroscience Emotion

I. Expression and Recognition of Emotion

The communication of emotion is very important for human interactions. We display emotions by our actions, and perceive it in others by the interpretation of those actions.

The scientific study of human emotional expression and recognition depends on the use of human subjects.

Our understanding of human emotion comes from: a) behavioral studies in normal subjects b) behavioral studies of patients with brain lesions c) imaging studies (PET & fMRI) of normals & brain-lesioned patients

What are the behavioral components by which we express and recognize human emotion? a) Facial expression b) Hand gesture c) Tone of voice d) Word choice

To study human emotion, subjects are asked to recognize emotional content in words or faces. They are asked to make judgments about emotional content in sentences and scenes.

A. Facial Expression

The ability to perform and perceive facial expressions is a very important part of human emotional communication.

Charles Darwin suggested that facial expressions are innate behavioral responses.

Support comes from the similarity of these expressions in cultures throughout the world. They are not culturally learned.

1 Also, blind children display normal facial expressions à again suggesting that they are not learned by observation.

Although facial expressions of emotion appear to be stereotyped behaviors, they can be modified by social context. Sometimes cultures impose restrictions on the expression of emotion.

A display rule is a cultural norm that modifies the expression of emotion in different societal situations.

B. Neural Basis of Recognition

1. Studies of Hemispheric Difference

Some studies indicate that areas in the right hemisphere of the brain are selectively involved in emotional comprehension. a. Perceptual Studies in Normals

Tachistoscopic presentation of visual stimuli to one hemifield and dichotic listening are used to compare the effects of presentation of material to the left and right hemispheres.

The contralateral hemisphere to the side of presentation receives more specific information than the ipsilateral side.

Subjects are found to respond more quickly and with greater accuracy (i.e. fewer errors) in detecting emotional cues when stimuli are presented to the right hemisphere than the left hemisphere. b. Cortical Lesion Studies i. Patients with right hemisphere cortical lesions are impaired in recognizing the emotions expressed by facial expression and hand gesture. Ability to recognize facial expression is independent of ability to recognize faces.

Adolphs study: right hemisphere lesions à selective recognition impairment for negative emotions.

2 ii. Patients with lesions in right temporal-parietal junction (rTPJ) cortex are impaired in judging emotion expressed by tone of voice. c. Imaging Studies

PET recording of rCBF while subjects assessed emotional content of verbal input shows that the judgment of emotion from voice tone selectively activates right prefrontal cortex.

2. Other Brain Structures a. Amygdala

The amygdala is active when people perceive and recall emotional content.

It is also involved in emotional recognition: i. people with bilateral amygdala lesions are impaired in the ability to recognize facial expression of emotion. Impairment is particularly severe for recognition of negative emotions such as fear. ii. these people are also impaired in ability to assess threat from facial expression, as compared to normals. iii. normal subjects have elevated activity in the amygdala when viewing facial expressions of fear. b. Basal Ganglia

The basal ganglia appear to be specifically related to the ability to recognize facial expressions of a particular emotion, disgust. i. Impairment in the ability to recognize facial expressions of disgust found in patients with degeneration (Huntingon’s disease) or malfunction (obsessive-compulsive disorder) of basal ganglia. ii. Increased activity in basal ganglia in neuroimaging of subjects viewing facial expression of disgust.

3 C. Neural Basis of Expression

1. Cortical Control of Facial Expression

As noted earlier, the facial expression of emotion is largely innate and stereotyped.

Evidence suggests that these expressions involve different systems than those involved in voluntary control of facial muscles: a. Duchenne’s muscle (orbicularis oculi) contracts during a genuine smile, but not a contrived smile. b. Volitional facial paresis: partial paralysis of the facial musculature under voluntary control, but activity of same muscles is normal in expression of genuine emotions. Damage to primary motor cortex or its efferent pathways. c. Emotional facial paresis: voluntary control of facial musculature is normal, but facial expression of emotion is impaired. Damage to insular cortex or its efferent pathways.

2. Hemispheric Differences

As with recognition, facial expression of emotion has a stronger right hemisphere component. a. Chimerical face studies: stronger emotional content expressed by left half of face than right. b. Wada test studies: reduced emotional expression (i.e. less intense emotions described) when right hemisphere put to sleep as compared to baseline. c. Stroke patients: right-hemisphere lesions impair ability to accurately express emotion (facially & by tone of voice).

Also, patients with right-hemisphere damage show less concern for disabilities than those with left-hemisphere damage.

4 II. Theories of Emotion Generation

A. James-Lange Theory

William James and Carl Lange each proposed similar theories to explain emotional experience.

It involves a three-step process:

1. Emotion-producing situations initially produce somatic physiological responses, e.g. autonomic physiological changes, behavioral responses.

2. The brain receives sensory input from the viscera and muscles resulting from the peripheral activations.

3. Interpretation of this secondary sensory input leads to the feeling (experience) of emotion in higher brain regions, including the cerebral cortex.

James-Lange theory thus implies that people cannot feel an emotion without first having a bodily (somatic) response.

B. Cannon-Bard Theory

Cannon and Bard were Harvard physiologists who opposed the James- Lange theory on 5 major grounds: 1) total separation of viscera from the CNS does not eliminate emotional behavior. 2) the same visceral responses occur in very different emotional states – the sympathetic n.s. functions as a single unit, and somatic physiological responses to emotion-producing situations are thus not distinct enough to distinguish among different emotions. 3) the viscera are relatively insensitive to external stimulation. 4) somatic physiological processes are too slow to be the origin of different emotions. 5) artificial production of emotion-related visceral changes does not actually cause emotional experience.

5 Cannon and Bard thus objected to the James-Lange theory because of its postulate that the brain’s emotional response is secondary to the peripheral response. Instead, they proposed that emotion involves simultaneous but independent activity of the peripheral nervous system and the brain.

According to Cannon-Bard theory, the sympathetic n.s. coordinates the body’s reaction to the situation, and the brain simultaneously generates emotional feeling. Accordingly, emotional feeling does not need to follow visceral input to the brain, and should be intact when that visceral input is removed.

C. Appraisal Theory

In the various forms of appraisal theory, emotional processing depends on the interaction between the properties of a stimulus and the interpretation of those properties. For example, emotion may be a response to the evaluation by the brain of the benefits and harms represented by an external object. Thus, a cognitive appraisal, not necessarily conscious, precedes the somatic physiological response and feeling.

D. Singer-Schachter Theory

This theory (sometimes called James-Lange-Schachter theory) is a blend of James-Lange and appraisal theories.

Singer & Schachter proposed that cognitive appraisal of emotion follows visceral input to the brain, and that this appraisal is required before an emotion is experienced.

Evidence that visceral input to the brain is necessary for the experience of emotion comes from the study of paraplegic (spinal-cord-injury) patients (although this evidence is now considered controversial). It is claimed that these patients continue to express (learned) emotional responses, but with reduced emotional feeling. The subjective intensity of emotion experienced by these patients is reported to correspond to the level of the lesion: i.e., the higher the transection, the less emotion is experienced. This finding is explained by the hypothesis that the lower the transection, the greater the loss of visceral input to the brain, and hence the lower the emotional feeling.

6 Schachter and Singer administered adrenaline to volunteers, creating an ambiguous sense of arousal. These subjects would interpret the visceral changes produced by the drug according to the context in which they were put – e.g., they would say that they were experiencing feelings of fear if put in a context of fear, or say that their feelings were drug induced if told that they had received adrenaline.

E. Constructivist Theory

There are various forms of constructivist theory. They all suggest that emotion emerges from cognition, as guided by culture and language.

The constructivist theory of Barrett holds that emotions are concepts that are constructed by humans as we make meaning from sensory input coming from the internal environment (body) and external environment. First, a concept is constructed of primal bodily changes called core affect. Then, this core affect is categorized according to language-based emotion categories.

F. Evolutionary Psychology Theory

This approach proposes that emotions involve the (evolved) coordination of physiological changes, behavioral tendencies, cognitive appraisals, and emotional feelings. They are all orchestrated to produce adaptive (successful) behavior.

G. LeDoux Theory

According to LeDoux, two neural emotion systems operate in parallel. The first system generates emotional responses; the second generates the feelings of emotion. The first is a fast system that is hardwired by evolution to increase the likelihood of survival. The second is a slow system of learned conscious responses.

III. The Amygdala & Implicit Emotion

In both humans and other species, the amygdala plays a critical role in implicit emotion, as demonstrated by fear processing.

7 LeDoux is a prominent cognitive neuroscientist who has studied fear processing in the amygdala. Fear processing depends on the amygdala, and the amygdala plays a major role in the processing of all emotions.

A. Kluver-Bucy Syndrome

In 1937, Kluver & Bucy reported on bilateral temporal lobe destruction in monkeys that produced a dramatic behavioral syndrome: a) wild animals became tame b) flattening of emotions c) oral tendencies -- put all kinds of encountered objects in mouth d) became hypersexual -- great increase in sexual behavior & inappropriate mounting

It is now known that these results come from destruction of temporal pole & amygdala in particular.

B. Anatomy of the Amygdala

The amygdala is composed of numerous nuclei that are reciprocally connected to the hypothalamus. Thus, the amygdala is in a position to exert control over the hypothalamus, and over the many somatic responses that the latter controls.

The amygdala is also connected with: 1) the nucleus acumbens -- part of the basal ganglia involved in reward 2) the orbitofrontal cortex

3 nuclei of the amygdala are most important for emotion: (1) lateral nucleus (LA) (2) basal nucleus (B) (3) central nucleus (CE)

The LA projects to the B and the CE. The CE is the principal output nucleus of the fear system. The CE projects to many areas of forebrain, hypothalamus and brainstem that control: (1) behavioral fear responses (2) endocrine fear responses (3) autonomic fear responses

8 Damage to the CE interferes with the expression of all fear CRs. Thus, the CE orchestrates the collection of hard-wired responses that underlie defensive behavior.

IV. The Emotion of Fear

The study of fear conditioning in rodents has been very important for revealing the neurobiology of emotion.

The study of fear conditioning has focused on three aspects of fear: (1) how the brain learns to fear an object or situation (2) how learned fears can guide the acquisition of behaviors that allow avoidance of danger (3) how fear can strengthen the memory formation of significant life events

A. Learning to Fear

Pavlovian fear conditioning as a model system

Pavlovian fear conditioning of a rat involves exposing the animal to a neutral stimulus, such as a tone (called the Conditioned Stimulus – CS) in conjunction with an aversive stimulus, such as a brief electric shock (called the Unconditioned Stimulus – US). After as few as one CS-US pairing, the animal begins to elicit a range of conditioned responses (CRs) to the CS and to the context in which conditioning occurs.

In rats, the CR includes: (1) immobility (2) autonomic responses (e.g. increased heart rate, blood pressure) (3) endocrine responses (e.g. increased levels of circulating stress hormones) (4) potentiation of reflexes (e.g. increased acoustic startle response)

In short, with conditioning the CS elicits many of the same defensive responses as the US.

9 Basic circuits of fear conditioning

In auditory fear conditioning in the rat, CS information about the tone is transmitted to the auditory thalamus (medial division of medial geniculate nucleus, MGm & posterior intralaminar nucleus, PIN) and then to auditory cortex (area TE1 à TE3). The auditory thalamus and cortex send fiber projections to the lateral nucleus of the amygdala (LA), with glutamate as the transmitter.

Auditory fear conditioning depends on the pathway from the auditory thalamus to the amygdala, but not from the auditory cortex. However, the auditory cortex is required when the animal must discriminate between different auditory CSs for conditioning to occur.

The same cells in LA that receive inputs from MGm/PIN and TE3 also respond to foot shock, and thus may integrate information about the tone and shock during fear conditioning. Thus, the LA is important for fear acquisition.

Synaptic plasticity and fear conditioning

The LA appears to be an essential locus of plasticity for fear conditioning because: a) single neurons in the LA have been identified where pathways converge carrying CS and US information. b) the response of these cells to a CS is greatly increased following fear conditioning. c) fear conditioning is mediated by an associative LTP-like NMDA- based process in the LA.

Evidence for associative LTP in the LA: a) after artificial LTP induction (i.e. due to tetanic electrical stimulation), the CS evokes an enhanced response in LA. b) fear conditioning produces similar electrophysiological changes in LA c) associative LTP and fear conditioning in LA are sensitive to the same disruptive effects from noncontingent postsynaptic LA neuron depolarization d) fear conditioning is impaired by pharmacological blockade of NMDA receptors in the amygdala

10 Contextual fear conditioning

Animals can be trained to fear context (e.g. the physical environment) by conditioning with foot shock. Conditioning to context may accompany auditory fear conditioning or may occur on its own.

1. The amygdala appears to be critically involved in storing the memory of contextual fear conditioning. (a) Lesions of the amygdala that include both the LA and basal nucleus (B) disrupt both acquisition and expression of contextual fear conditioning. (b) contextual fear conditioning is also impaired by infusion of an NMDA receptor antagonist in the amygdala.

It is not yet known which nuclei of the amygdala are critical for the memory, but there is some evidence that the LA and anterior basal nucleus are involved. The CE must be intact for the expression of contextual fear.

2. The hippocampus also appears to play a role in contextual fear conditioning since lesions of hippocampus disrupt contextual fear conditioning.

However, it is disrupted only by lesions that occur shortly after conditioning. There appears to be a period of consolidation that requires hippocampal involvement. Presumably, the contextual information is consolidated in the neocortex.

It is hypothesized that the hippocampus is involved in 2 ways: (a) to first form a representation of the context in which the conditioning will occur (b) to then provide the amygdala with contextual information during CS- US training

Anatomy: the hippocampus projects to the basal nucleus of the amygdala.

Immediate shock is not sufficient to support contextual fear conditioning. But, if the animal is exposed to the conditioning environment prior to training, then contextual fear conditioning is possible following immediate shock. This indicates that the contextual representation must already be formed prior to the fear conditioning.

11 Retrieval and reactivation of fear memories

Memory retrieval may make the retrieved material susceptible to disruption in a manner similar to a newly formed memory.

Following active recall of a fear memory, there appears to be a period of re- consolidation that requires protein synthesis in the amygdala: infusion of a protein synthesis inhibitor into the amygdala immediately after retrieval of auditory fear memory impairs memory recall on subsequent tests.

Hippocampal-dependent contextual memories also appear to be sensitive to disruption at the time of retrieval.

It appears that hippocampal-independent contextual memory must return to the hippocampus during retrieval and undergo a protein synthesis- dependent reconsolidation in order to be retained.

B. The Role of Fear in Danger Avoidance

In instrumental (operant) fear learning, the animal learns to detect dangerous objects or situations, and also uses the learned information to guide ongoing behavior to actually avoid danger. The amygdala appears to play a role in instrumental fear conditioning, as it does in Pavlovian fear conditioning.

The projection from the LA to the basal nucleus appears to be involved in instrumental fear conditioning.

In an escape-from-fear task: a) lesion of LA disrupted both the Pavlovian and the instrumental components of the task b) lesion of CE impaired only the Pavlovian component c) lesion of B impaired only the instrumental component

The basal nucleus of the amygdala may guide fear-related instrumental conditioning through its projections to the basal ganglia.

12 C. Strengthening of Memory Formation by Fear

Remember the distinction between implicit and explicit learning, and that Pavlovian fear conditioning is a form of implicit learning.

However, in real-world situations Pavlovian fear conditioning may most often occur along with explicit learning.

Explicit memory formation is believed to depend on the medial temporal lobe memory system, consisting of the hippocampus and related cortical areas, e.g. parahippocampal cortex, entorhinal cortex, etc. During fearful (or other emotion-laden) experience, one route by which the amygdala can influence explicit memory formation is by its projections to the hypothalamus.

The amygdala can drive the hypothalamic-pituitary-adrenal (HPA) axis.

1. The hypothalamus releases corticotrophin releasing factor (CRF) into specialized blood vessels serving the anterior pituitary gland. 2. The anterior pituitary is stimulated to release a number of different hormones into the general circulation. One of these is adrenocorticotrophic hormone (ACTH). 3. ACTH acts on the adrenal cortex to release glucocorticoids (including cortisol) into the general circulation. 4. Glucocorticoids can cross the blood-brain barrier, and modulate the function of amygdala, hippocampus and/or neocortex.

5. In addition to affecting the hippocampus hormonally, the amygdala sends direct axonal projections to it.

13 In inhibitory avoidance learning: 1) immediate post-training blockade of glucocorticoid receptors in the amygdala impairs memory acquisition. 2) facilitation of those receptors enhances memory acquisition.

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