Amygdala - Emotion Generator And Regenerator
Striking points:
(1) The amygdala is a tiny collection of nuclei that receives inputs from the thalamus, hippocampus, and neocortex and sends many of its outputs to structures that produce excitatory neurotransmitters, most of which are in the brainstem.
(2) Stress triggers physiological states of emotion, which in turn contribute to the stress response.
(3) During wakefulness, the amygdala generates emotions which are mainly utilized to predict the potential stress associated with a potential experience and engage or avoid it as necessary.
(4) During rapid eye movement (REM) sleep, the amygdala again regenerates emotions that are similar to the emotional states of wakefulness but lacking in noradrenaline, so as to reprocess and depotentiate the stress associated with a stressful experience thereby increasing the ability of the individual to cope with similar stressful experiences more successfully in the future.
(1) The amygdala is a tiny collection of nuclei that receives inputs from the thalamus, hippocampus, and neocortex and sends many of its outputs to structures that produce excitatory neurotransmitters, most of which are in the brainstem.
(2) Stress triggers physiological states of emotion, which in turn contribute to the stress response.
(3) During wakefulness, the amygdala generates emotions which are mainly utilized to predict the potential stress associated with a potential experience and engage or avoid it as necessary.
(4) During rapid eye movement (REM) sleep, the amygdala again regenerates emotions that are similar to the emotional states of wakefulness but lacking in noradrenaline, so as to reprocess and depotentiate the stress associated with a stressful experience thereby increasing the ability of the individual to cope with similar stressful experiences more successfully in the future.
Opening
A tiny structure, the amygdala is hard to see even when one is looking straight at it. It differs from the other brain structures in that its primary role is to generate physiological states rather than process information.
Amygdala And Projections
The amygdala consists of a pair of almond-shaped structures lying deep within the medial temporal lobe, adjacent to the hippocampus. It is small, averaging a width of 15 mm and an only slightly longer length (Zald, 2003); interestingly, the human amygdala reaches adult volume by age 4 years in females but may continue to grow until age 18 years in males (Giedd et al, 1996). Like most brain structures, the amygdala is a collection of somewhat ambiguous nuclei that can be classified a number of different ways, though this has no effect on how they perform their functions. To reduce ambiguity, we will focus on only the main components here.
(1) Basolateral amygdala. The basolateral amygdala (BLA) is the almond-shaped structure that originally defined the amygdala; it consists of cortex-like nuclei, similar in organization and cell composition to the neocortex (Lee et al, 2013). The BLA displays astonishingly promiscuous connectivity (Pare, 2003). The BLA is the synaptic interface of the amygdala and receives visual, auditory, and somatosensory inputs from the hippocampus, neocortex, and thalamus. These inputs form synaptic connections with the dendrites of principal neurons which then send outputs directly back to the hippocampus, entorhinal region of the neocortex, and thalamus, as well as to the nucleus accumbens in the striatum of the basal nuclei (Davis and Whalen, 2001). In addition to these direct projections, the BLA projects indirectly to the hypothalamus and multiple brainstem areas via another part of the amygdala called the central nucleus. The inputs and outputs of the BLA involve the excitatory neurotransmitter glutamate. (2) Central nucleus. The central nucleus (CEA) consists of striatal-like nuclei, with neurons that have similar morphological, physiological, and biomechanical properties to the medium spiny neurons of the striatum of the basal nuclei (Lee et al, 2013). The CEA is the output region of the amygdala; it receives inputs from the BLA and then sends outputs to the hypothalamus, basal nucleus of Meynert in the forebrain (produces acetylcholine), and multiple brainstem target areas including the reticular formation raphe nuclei (produce serotonin), the periaqueductal gray (PAG, behavioural control interface) and ventral tegmental area (VTA, produces dopamine) of the midbrain, and the locus coeruleus (produces noradrenaline) of the pons. Like the striatum, the neurons projecting from the CEA use the inhibitory neurotransmitter gamma-amino butyric acid (GABA). (3) Intercalated cell masses. There are multiple intercalated cell masses (ITCs) that regulate the BLA and CEA, as well as the projections between the amygdala and other brain structures (Lee et al, 2013). The ITCs are located along the borders of the BLA and provide feedforward inhibition using the neurotransmitter GABA. (4) Amygdala structural organization. Thus, sensory information from the hippocampus, neocortex, and thalamus flows into the BLA and is relayed directly, or indirectly via the CEA, to other brain regions. Through the CEA, the amygdala can facilitate the release of noradrenaline, acetylcholine, serotonin, and dopamine throughout the rest of the brain. Moreover, since receptors for these neurotransmitters are differentially distributed throughout the amygdala nuclei, they can modulate the flow of information through the amygdala itself by influencing excitatory and inhibitory neuron interactions (LeDoux, 2008). |
The amygdala is an almond-shaped structure (red) that lies deep within the medial temporal lobe, adjacent to the seahorse-shaped hippocampus (blue).
It is difficult to see the amygdala in a real brain.
This is a simplified diagram of the amygdala and its projections; some surrounding nuclei and projections have been sacrificed for clarity. The main amygdala components are the BLA (red), the CEA (pale orange), and ITCs (gray). Sensory information from the hippocampus, neocortex, and thalamus arrives at the BLA, after which it is sent directly to the hippocampus, neocortex, nucleus accumbens of the basal nuclei, and thalamus, or indirectly via the CEA to the hypothalamus, basal nucleus of Meynert, and brainstem. Projections to and from the BLA use glutamate and are excitatory (blue markers) while projections from the CEA use GABA and are inhibitory (brown markers).
Through the CEA, the amygdala can facilitate the release of many different neurotransmitters including noradrenaline, acetylcholine, serotonin, and dopamine; each of these neurotransmitters has widespread effects on many brain structures, including the amygdala itself.
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Stress And Emotion
The world is full of different experiences, some of which elicit stress; in humans, stressful experiences almost always trigger an emotion. Stress and emotion are both physiological states that enhance memory formation; the former affects the body whereas the latter primarily affects the brain.
(1) Stress. If the individual experiences a challenge that overwhelms their coping resources, a physiological state of stress occurs in the body. Stress is initiated by the amygdala which via the hypothalamus stimulates the release of the stress hormones cortisol and adrenaline by the adrenal glands, which in turn activate the amygdala even further; cortisol crosses the blood-brain barrier to directly stimulate BLA cortisol receptors whereas adrenaline indirectly stimulates the BLA via the vagus nerve (Pare, 2003). Through the BLA to CEA pathway, the activated amygdala also stimulates the release of noradrenaline by the locus coeruleus, acetylcholine by the basal nucleus of Meynert, serotonin by the raphe nuclei, and dopamine by the VTA. Various physical effects are produced by stress, such as increased heart rate and pupil dilation. The physiological changes induced by stress are temporary; in cats exposed to shock, the BLA neuron firing rate peaks by 30 to 50 minutes and subsides by two hours (Pelletier et al, 2005). However, they result in more lasting structural and behavioural changes. Structurally, rats subjected to prolonged immobilization show synaptic modification and dendritic growth in the BLA principal neurons, changes that also occur in concert with structural changes in the hippocampus (Roozendaal, 2009). Behaviourally, the rats show an increase in anxiety-like behaviour, but they also display - and this has been shown in humans too - increased memory formation at the cost of impaired working memory and memory retrieval (Roozendaal, 2009). Noradrenaline plays a central role in enhancing memory formation - as an example, noradrenaline infusions into the BLA of rats after a water maze task enhances the memory of the task, whereas beta-blocking medications impair this process (Hatfield and McGaugh, 1999). (2) Emotion. There are numerous definitions for emotion out there, but for now we shall define emotion as a physiological state within the brain that occurs after stress. The amygdala is crucially involved in emotion; in monkeys, amygdala lesions disrupt emotional behaviour whereas lesions involving the nearby perirhinal and parahippocampal cortices impair memory but not emotional behaviour (Zola-Morgan et al, 1989). The BLA receives sensory information largely from two sources - the neocortex, via a cortical route that delivers slow yet highly processed information, and the thalamus, via a subcortical route that delivers rapid yet unprocessed information (Lee et al, 2013); we'll discuss these two routes more later. Regardless of which route is taken, when sensory information relating to a stressful experience arrives at the BLA and an emotion is produced, a physiological state similar to that of stress is initiated with increased BLA neuron firing rates and increased levels of noradrenaline, acetylcholine, serotonin, and dopamine (Pare, 2003). However, emotional arousal is also accompanied by synchronized theta oscillations involving the BLA, hippocampus, and entorhinal cortex such that much of the temporal lobe oscillates at theta frequency during emotional arousal (Pare and Gaudreau, 1996; Alonso and Garcia-Austt, 1987); this temporal lobe resonance underlies emotion. Just like thalamocortical resonance during states of attention facilitates synaptic modification in the entire neocortex, temporal lobe resonance during states of emotional arousal probably facilitates synaptic modification in the amygdala, hippocampus, and entorhinal cortex and it has indeed been shown that emotional arousal during an experience enhances encoding and consolidation (Pare, 2003) - for example, rats with BLA lesions performed before or within two days of learning an inhibitory avoidance response show impaired memory retention, although lesions performed ten days after learning have no effect on retention (Liang et al, 1982); therefore while the amygdala enhances memory formation, it does not store memories. |
The stress or "fight or flight" response occurs after a threat or challenge to one's well-being is experienced. The amygdala initiates the stress response which via the hypothalamus stimulates the release of stress hormones such as cortisol and adrenaline; these activate the amygdala further, resulting in the release of additional neurotransmitters and various physical effects. These physiological changes and physical effects are temporary, but result in more lasting structural and behavioural changes.
The neurotransmitter noradrenaline plays an important role in memory formation - infusions into the BLA of rats after a water maze task enhances memory of the task whereas beta-blocking medications impair memory for the task (Hatfield and McGaugh, 1999).
The amygdala generates emotion - in monkeys, amygdala lesions disrupt emotional behaviour but lesions of the nearby perirhinal and parahippocampal cortices do not (Zola-Morgan et al, 1989).
Contrasting stress with emotion.
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Generating Emotions To Predict Stress
We now speculate on the mechanism by which the amygdala contributes to information processing. The amygdala generates emotional states, which until now we have defined as physiological states within the brain
that occur after stress. We will now expand this definition to include physiological states that may occur before a potential stress; emotions in this sense provide a survival advantage by predicting whether a
potential experience will be stressful or not, so that it may be avoided or not.
(1) Generating emotions after stress. We spoke about the mechanisms of stress and emotion earlier, and how the former triggers the latter. There is a lot of evidence that physiological states of stress almost always triggers physiological states of emotion, most of which revolves around the study of pain triggering fear. Amygdala responses to aversive stimuli such as pain are consistent - the greater the pain, the greater the amygdala activation and resulting emotional arousal (Zald, 2003). Perhaps the simplest and most powerful of all emotions is fear; if a child first experiences a snakebite, fear conditioning occurs as the snake transforms from an emotionally neutral stimulus into one that elicits fear and subsequent defensive behaviour. The amygdala is crucial to fear conditioning as patients with amygdala damage fail to show a physiological fear response, but if their hippocampus is intact they can remember and report the events of fear-conditioning procedures; likewise, patients with hippocampus damage fail to report the events of fear-conditioning, but if their amygdala is intact there is a physiological fear response (Bechara et al, 1995; LaBar et al, 1995; Phelps and LeDoux, 2005). (2) Generating emotions before a potential stress. While stress triggers emotion, simply having an emotional response to something does not aid the survival of the individual; emotion probably evolved for a reason. Many studies show that activation of the amygdala facilitates states of attention by contributing to the neocortical activation that is stimulated by the thalamus during thalamocortical resonance. The amygdala can activate the neocortex both directly and indirectly. Directly, there are reciprocal connections between the amygdala and neocortex by which direct stimulation of the neocortex into a more activated state may occur (Phelps and LeDoux, 2005). Indirectly, the CEA projects to the basal nucleus of Meynert which in turn projects to widespread neocortical areas where it releases the excitatory neurotransmitter acetylcholine (Phelps and LeDoux, 2005); it has been shown in several animal species that electrical stimulation of the CEA increases attention or processes associated with increased attention (Davis and Whalen, 2001). By facilitating attention, the amygdala selectively enhances the encoding and consolidation of memories resulting in less forgetting over time (Berlyne and Carey, 1968; Kleinsmith and Kaplan, 1963), particularly memories that involve novelty or are associated with a known reward or stress. It is important to pay more attention to things that are novel and therefore potentially rewarding or stressful, as well as things that are known to be rewarding or stressful, as these things have the most immediate impact on survival. (a) Facilitating attention towards novel things. The thalamus and hippocampus are readily activated when novel sensory information passes unrecognized and unmatched up the neocortical hierarchy. However, novel sensory information activates the amygdala too (Zald, 2003), resulting in facilitated attention towards novel things - for example, the amygdala activates during the viewing of unusual scenes, such as surreal images, compared to ordinary scenes, such as plants (Hamann et al, 2002); the more bizarre the scene, the more the amygdala activates (Rotshtein et al, 2001). Recall that the amygdala receives most of its sensory information from either the thalamus or neocortex; since novel sensory information can only be identified as novel after passing unrecognized through the neocortex, novel sensory information enters both the hippocampus and amygdala through a relatively slow yet highly processed cortical route, a route that is accessible to awareness; we will discuss awareness in chapter eight. (b) Facilitating attention towards rewarding or stressful things. The amygdala also facilitates attention towards known rewarding or stressful things during memory formation (Phelps, 2004; Zald, 2003). It has been shown that the amygdala activates to reward-related stimuli, such as viewing erotic images or anticipating delicious food (Karama et al, 2002; Zald, 2003). The amygdala also activates to potentially stressful, emotionally arousing stimuli as demonstrated by the attentional blink phenomenon (Anderson and Phelps, 2001). In normal subjects given two target stimuli presented one right after the other in a stream of rapidly presented stimuli, the second target will be missed, as if attention "blinked", but if the second target is emotionally arousing, such as a dirty word, it is less likely to be missed. In subjects with amygdala lesions, however, it will still likely be missed, even if it is emotionally arousing. Interestingly, neither awareness nor an intact visual neocortex are required to identify stressful emotional stimuli - for example, amygdala activation to fear versus neutral faces does not depend on whether or not the subjects are aware of the faces (Whalen et al, 1998) or whether or not the faces are the focus of attention (Vuilleumier et al, 2001; Anderson et al, 2003; Williams et al, 2004), and amygdala activation still occurs to fear versus neutral faces in patients with a condition called blindsight in which the visual cortex is so damaged that the patient is blind yet can respond to certain visual stimuli (Morris et al, 2001; Pegna et al, 2005). Thus, sensory information pertaining to a known reward or stress probably enters the amygdala through a rapid yet relatively unprocessed subcortical route of processing, a route that involves the amygdala, thalamic pulvinar nucleus, and midbrain superior colliculus; recall from chapter two that the superior colliculus used to be a much larger structure called the optic tectum which may explain how certain visual stimuli can be detected in blindsight. This subcortical route activates to emotional facial expressions before subjects are even aware of them (Morris et al, 1998). By subcortically detecting known rewarding and stressful things before the neocortex has had a chance to fully process them and decide what to do, the decision as to whether to engage or avoid them can be made instantly. (3) The absence of stress. Until now, we have seen that the amygdala activates before, during, or after a stressful experience. However, in situations lacking stress, amygdala activity actually decreases - for example, pleasant stimuli such as "chill" inducing music, viewing happy faces, or viewing the faces of loved ones is associated with a decrease in amygdala activity (Bartels and Zeki, 2000; Blood and Zatorre, 2002; Morris et al, 1996; Zald, 2003). Presumably, each of these pleasant experiences activated the amygdala when they were initially encountered as novelty, but after some time the amygdala depotentiated its response as despite repeated exposure, no significant stress ever eventuated; this depotentiation will be discussed in the next section. |
The amygdala activates after stress, and then prior to that stress in the future. Pain from a snakebite activates the amygdala and generates the emotion of fear afterwards as fear conditioning transforms the snake form an emotionally neutral stimulus into one that elicits fear. The next time a snake is sensed, the amygdala activates and generates fear prior to any potential bite so that the stress of the bite can be avoided.
The amygdala activates the neocortex both directly and indirectly. Directly, the excitatory glutaminergic neurons of the BLA activate the neocortex. Indirectly, the ITCs inhibit the inhibitory GABAergic neurons of the CEA so that the basal nucleus of Meynert releases more excitatory acetylcholine, activating the neocortex.
The amygdala activates more to unusual, novel stimuli, such as this surreal image created by Salvador Dali.
Novel things can only be identified as novel after the relevant sensory information has passed unrecognized through the neocortex; the amygdala facilitates attention towards novel things by being activated through a relatively slow, highly processed cortical route accessible to awareness.
In the attentional blink phenomenon, normal subjects asked to notice the face followed by the clock in a stream of images presented rapidly will miss the clock most of the time, as if attention "blinked".
In normal subjects, if the second target is emotionally arousing such as a dirty word, it is less likely to be missed. However in patients with amygdala lesions, the dirty word will still be missed.
The amygdala also facilitates attention towards emotional stimuli related to reward and stress by being activated through a rapid, relatively unprocessed subcortical route not accessible to awareness. The subcortical route involves the amygdala, thalamic pulvinar nucleus, and midbrain superior colliculus (Morris et al, 1998).
In viewing the face of a loved one such as your grandmother, there is no novelty, reward, or stress and so the amygdala does not activate.
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Regenerating Emotions To Cope With Stress
The amygdala regenerates emotions in rapid eye movement (REM) sleep so as to depotentiate the stress of prior stressful experiences, allowing the individual to cope with similar experiences more successfully in the future. REM sleep is also associated with an active neocortex, a circumvented basal nuclei, and an inhibited hippocampus as we discussed in previous chapters.
(1) REM dreams. Dreaming is prolific in REM sleep, with a recall rate of over 80% compared to 50% for NREM sleep (Nielsen, 2000). Compared to NREM dreams, REM dreams are abstract; they are fragmented, bizarre, and laden with emotion, containing things from both the recent and distant past but lacking the context in which they were experienced (Purves and Fitzpatrick, 2001; Wamsley and Stickgold, 2011). Using fear as an example, an experience that produced fear might not appear in a REM dream over the next few nights, but elements of other previous fearful experiences in the recent or even distant past might be used to construct a fragmented and bizarre narrative during REM sleep, the common tie binding the actual experience with the REM dream would be the regeneration of the emotion of fear. (2) Regenerating emotions to cope with stress. We mentioned earlier how the amygdala generates temporal lobe resonance; during REM sleep, the pontine reticular formation also contributes to the generating and enhancing of theta wave synchronization between the BLA and hippocampus (Karashima et al, 2010). Thus, the amygdala and pontine reticular formation probably both contribute to regenerating emotions during REM sleep. These regenerated emotions are physiologically different compared to the emotions of wakefulness, the main difference being that while both contain high levels of acetylcholine, noradrenaline levels are high in wakefulness but negligible in REM sleep (Dubuc, 2014). Most of the emotional content in REM dreams is highly stressful, with 65% of dreams associated with sadness, apprehension, or anger (Purves and Fitzpatrick et al, 2001). These low noradrenaline levels may thus allow previously stressful experiences to be reprocessed and "depotentiated" such that the next time the same or a similar stressful experience is encountered, the stress and subsequent emotional intensity are reduced (van der Helm et al, 2011). In support of this idea, it has been shown in humans that a night of sleep reduces amygdala activity and subjective emotional reactivity to previously encountered stimuli (Rasch and Born, 2013; van der Helm et al, 2011), and BLA damage in rats prevents the ability to actively cope (regulate the emotional response) with regards to fearful stimuli (Amorapanth et al, 2000; Phelps and LeDoux, 2005). Thus, the amygdala regenerates emotions during REM sleep so as to increase the ability of the individual to cope with stress. Interestingly, depressed patients have a higher proportion of REM sleep than non-depressed subjects (Rasch and Born, 2013); emotional tone attenuation may not be functional in patients with depression. |
REM dreams are laden with emotion, extremely fragmented, and bizarre, containing memories remotely related to past experiences. However, while the experiences in reality and REM dream may differ, they are strongly connected by the reproduction of the same emotion. If someone was threatened by a person with a knife, perhaps they would later dream of Freddy Krueger and his blades, who they saw in a movie years ago; the images are different and remotely related, but the same emotion, fear, is reproduced in each.
The amygdala produces emotional states during wakefulness, but together with the pontine reticular formation it also regenerates emotional states during REM sleep that display physiologically differences. In wakefulness, levels of noradrenaline (top) and acetylcholine (bottom) are both high (Dubuc, 2014). In NREM sleep, they are both low. In REM sleep, noradrenaline levels are low but acetylcholine levels are high so while an emotional experience can be re-experienced, the associated is removed such that the stress of the experience is depotentiated.
By depotentiating the stress associated with a particular experience, REM sleep increases the coping ability of the individual for similarly stressful experiences in future; a night of sleep has been shown in humans to reduce amygdala activity and subjective emotional reactivity to previously encountered stimuli (van der Helm et al, 2011).
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Closing
The amygdala generates and regenerates emotional states. Emotion is not an end in itself; it evolved for good reason and can warn the individual about a potentially stressful experience quickly, before the neocortex has even processed it, and without having to experience that stress.
References
Anderson and Phelps. 2001. The human amygdala supports affective modulatory influences on visual awareness. Nature 411, 305-309.
Anderson et al. 2003. Neural correlates of the automatic processing of threat facial signals. Journal of Neuroscience 23, 5627-5633.
Alonso and Garcia-Austt. 1987. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. Experimental Brain Research 67, 493-501.
Amorapanth et al. 2000. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nature Neuroscience 3, 74-79.
Bartels and Zeki. 2000. The neural basis of romantic love. Neuroreport 11, 3829-3834.
Bechara et al. 1995. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115-1118.
Berlyne and Carey. 1968. Incidental learning and the timing of arousal. Psychonomic Science 13(2), 103-104.
Blood and Zatorre. 2001. Intensely pleasurably responses to music correlate with activity in brain regions implicated in reward and emotion. Proceedings of the National Academy of Sciences 98, 11818-11823.
Davis and Whalen. 2001. The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13-34.
Dubuc. 2014. The Brain From Top To Bottom. http://thebrain.mcgill.ca/flash/i/i_11/i_11_cr/i_11_cr_cyc/i_11_cr_cyc.html.
Giedd et al. 1996. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. Journal of Comparative Neurology 366, 223-230.
Hamann et al. 2002. Kilts, ecstasy and agony: activation of the human amygdala in positive and negative emotion. Psychological Science 13, 135-141.
Hatfield and McGaugh. 1999. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of Learning and Memory 71, 232-239.
Karama et al. 2002. Areas of brain activation in males and females during viewing of erotic film excerpts. Human Brain Mapping 16, 1-13.
Kleinsmith and Kaplan. 1963. Paired-associate learning as a function of arousal and interpolated interval. Journal of Experimental Psychology 65, 190-193.
LaBar et al. 1995. Impaired fear conditioning following unilateral temporal lobectomy in humans. Journal of Neuroscience 15, 6846-6855.
LeDoux. 2008. Amygdala. Scholarpedia 3(4), 2698.
Lee et al. 2013. Inhibitory networks of the amygdala for emotional memory. Frontiers in Neural Circuits 7(129), 1-10.
Liang et al. 1982. Post-training amygdala lesions impair retention of an inhibitory avoidance response. Behavioural Brain Research 4, 237-249.
Morris et al. 1996. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812-815.
Morris et al. 1998. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47-57.
Morris et al. 2001. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241-1252.
Nielsen. 2000. A review of mentation in REM and NREM sleep: "covert" REM sleep as a possible reconciliation of two opposing models. Behavioural and Brain Sciences 23, 851-866, 904-1121.
Pare. 2003. Role of the basolateral amygdala in memory consolidation. Progress in Neurobiology 70, 409-420.
Pare and Gaudreau. 1996. Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. Journal of Neuroscience 16, 3334-3350.
Pegna et al. 2005. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neuroscience 8, 24-25.
Pelletier et al. 2005. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learning and Memory 12, 96-102.
Phelps. 2004. Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology 14, 198-202.
Phelps and LeDoux. 2005. Contributions of the amygdala to emotion processing: from animal models to human behaviour. Neuron 48, 175-187.
Purves and Fitzpatrick. 2001. The possible functions of REM sleep and dreaming. Neuroscience, 2nd Edition. Sinauer Associates.
Rasch and Born. 2013. About sleep's role in memory. Physiological Reviews 93(2), 681-766.
Roozendaal. 2009. Stress, memory, and the amygdala. Nature Reviews Neuroscience 10(6), 423-433.
Rotshtein et al. 2001. Feeling or features: different sensitivity to emotion in high-order visual cortex and and amygdala. Neuron 32, 747-757.
van der Helm et al. 2011. REM sleep de-potentiates amygdala activity to previous emotional experiences. Current Biology 21(23), 2029-2032.
Vuilleumier et al. 2001. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829-841.
Wamsley and Stickgold. 2011. Memory, sleep and dreaming: experiencing consolidatoin. Sleep Medicine Clinics 6(1), 97-108.
Whalen et al. 1998. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 18, 411-418.
Williams et al. 2004. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. Journal of Neuroscience 24, 2898-2904.
Zald. 2003. The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews 41, 88-123.
Zola-Morgan et al. 1989. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience 9(12), 4355-4370.
Anderson and Phelps. 2001. The human amygdala supports affective modulatory influences on visual awareness. Nature 411, 305-309.
Anderson et al. 2003. Neural correlates of the automatic processing of threat facial signals. Journal of Neuroscience 23, 5627-5633.
Alonso and Garcia-Austt. 1987. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. Experimental Brain Research 67, 493-501.
Amorapanth et al. 2000. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nature Neuroscience 3, 74-79.
Bartels and Zeki. 2000. The neural basis of romantic love. Neuroreport 11, 3829-3834.
Bechara et al. 1995. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115-1118.
Berlyne and Carey. 1968. Incidental learning and the timing of arousal. Psychonomic Science 13(2), 103-104.
Blood and Zatorre. 2001. Intensely pleasurably responses to music correlate with activity in brain regions implicated in reward and emotion. Proceedings of the National Academy of Sciences 98, 11818-11823.
Davis and Whalen. 2001. The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13-34.
Dubuc. 2014. The Brain From Top To Bottom. http://thebrain.mcgill.ca/flash/i/i_11/i_11_cr/i_11_cr_cyc/i_11_cr_cyc.html.
Giedd et al. 1996. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. Journal of Comparative Neurology 366, 223-230.
Hamann et al. 2002. Kilts, ecstasy and agony: activation of the human amygdala in positive and negative emotion. Psychological Science 13, 135-141.
Hatfield and McGaugh. 1999. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of Learning and Memory 71, 232-239.
Karama et al. 2002. Areas of brain activation in males and females during viewing of erotic film excerpts. Human Brain Mapping 16, 1-13.
Kleinsmith and Kaplan. 1963. Paired-associate learning as a function of arousal and interpolated interval. Journal of Experimental Psychology 65, 190-193.
LaBar et al. 1995. Impaired fear conditioning following unilateral temporal lobectomy in humans. Journal of Neuroscience 15, 6846-6855.
LeDoux. 2008. Amygdala. Scholarpedia 3(4), 2698.
Lee et al. 2013. Inhibitory networks of the amygdala for emotional memory. Frontiers in Neural Circuits 7(129), 1-10.
Liang et al. 1982. Post-training amygdala lesions impair retention of an inhibitory avoidance response. Behavioural Brain Research 4, 237-249.
Morris et al. 1996. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812-815.
Morris et al. 1998. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47-57.
Morris et al. 2001. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241-1252.
Nielsen. 2000. A review of mentation in REM and NREM sleep: "covert" REM sleep as a possible reconciliation of two opposing models. Behavioural and Brain Sciences 23, 851-866, 904-1121.
Pare. 2003. Role of the basolateral amygdala in memory consolidation. Progress in Neurobiology 70, 409-420.
Pare and Gaudreau. 1996. Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. Journal of Neuroscience 16, 3334-3350.
Pegna et al. 2005. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neuroscience 8, 24-25.
Pelletier et al. 2005. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learning and Memory 12, 96-102.
Phelps. 2004. Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology 14, 198-202.
Phelps and LeDoux. 2005. Contributions of the amygdala to emotion processing: from animal models to human behaviour. Neuron 48, 175-187.
Purves and Fitzpatrick. 2001. The possible functions of REM sleep and dreaming. Neuroscience, 2nd Edition. Sinauer Associates.
Rasch and Born. 2013. About sleep's role in memory. Physiological Reviews 93(2), 681-766.
Roozendaal. 2009. Stress, memory, and the amygdala. Nature Reviews Neuroscience 10(6), 423-433.
Rotshtein et al. 2001. Feeling or features: different sensitivity to emotion in high-order visual cortex and and amygdala. Neuron 32, 747-757.
van der Helm et al. 2011. REM sleep de-potentiates amygdala activity to previous emotional experiences. Current Biology 21(23), 2029-2032.
Vuilleumier et al. 2001. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829-841.
Wamsley and Stickgold. 2011. Memory, sleep and dreaming: experiencing consolidatoin. Sleep Medicine Clinics 6(1), 97-108.
Whalen et al. 1998. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 18, 411-418.
Williams et al. 2004. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. Journal of Neuroscience 24, 2898-2904.
Zald. 2003. The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews 41, 88-123.
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