Biology:Affective neuroscience

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Short description: Study of the neural mechanisms of emotion
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Affective neuroscience is the study of the neural mechanisms of emotion. This interdisciplinary field combines neuroscience with the psychological study of personality, emotion, and mood.[1] The putative existence of 'basic emotions' and their defining attributes represents a long lasting and yet unsettled issue in the field.[2]

The term was coined by neuroscientist Jaak Panksepp, at a time when cognitive neuroscience focused on non-emotional cognition, such as attention or memory.

Brain areas

Emotions are thought to be related to activity in brain areas that direct our attention, motivate our behavior, and choose the significance of what is going on around us. Pioneering work by Paul Broca (1878),[3] James Papez (1937),[4] and Paul D. MacLean (1952)[5] suggested that emotion is related to a group of structures in the center of the brain called the limbic system, which includes the hypothalamus, cingulate cortex, hippocampi, and other structures. Research has shown that limbic structures are directly related to emotion, but other structures have been found to be of greater emotional relevance. The following brain structures are currently thought to be involved in emotion:[6]

Limbic system

  • Amygdala – The amygdalae are two small, round structures located anterior to the hippocampi near the temporal poles. The amygdalae are involved in detecting and learning which parts of our surroundings are important and have emotional significance. They are critical for the production of emotion, and may be particularly so for negative emotions, especially fear.[7] Multiple studies have shown amygdala activation when perceiving a potential threat; various circuits allow the amygdala to use related past memories to better judge the possible threat.[8]
  • Thalamus – The thalamus is involved in relaying sensory and motor signals to the cerebral cortex,[9] especially visual stimuli. The thalamus plays an important role in regulating states of sleep and wakefulness.[10]
  • Hypothalamus – The hypothalamus is involved in producing a physical output associated with an emotion as well as in reward circuits.[11]
  • Hippocampus – The hippocampus is a structure of the medial temporal lobes that is mainly involved in memory. It works to form new memories and also connects senses such as visual input, smell or sound to memories. The hippocampus allows long term memories to be stored and retrieves them when necessary. Memories are used within the amygdala to help evaluate stimuli.[12]
  • Fornix – The fornix is the main output pathway from the hippocampus to the mammillary bodies. It has been identified as a main region in controlling spatial memory functions, episodic memory and executive functions.[13]
  • Mammillary body – Mammillary bodies are important for recollective memory.[14]
  • Olfactory bulb – The olfactory bulbs are the first cranial nerves, located on the ventral side of the frontal lobe. They are involved in olfaction, the perception of odors.[15]
  • Cingulate gyrus – The cingulate gyrus is located above the corpus callosum and is usually considered to be part of the limbic system. The parts of the cingulate gyrus have different functions, and are involved with affect, visceromotor control, response selection, skeletomotor control, visuospatial processing, and in memory access.[16] A part of the cingulate gyrus is the anterior cingulate cortex, which is thought to play a central role in attention[17] and behaviorally demanding cognitive tasks.[18] It may be particularly important with regard to conscious, subjective emotional awareness. This region of the brain may play an important role in the initiation of motivated behavior.[18] The subgenual cingulate is more active during both experimentally induced sadness and during depressive episodes.[19]

Other brain structures

  • Basal ganglia – Basal ganglia are groups of nuclei found on either side of the thalamus. Basal ganglia play an important role in motivation,[20] action selection and reward learning.[21]
  • Orbitofrontal cortex – The orbitofrontal cortex is a major structure involved in decision making and the influence by emotion on that decision.[22]
  • Prefrontal cortex – The prefrontal cortex is the front of the brain, behind the forehead and above the eyes. It appears to play a critical role in the regulation of emotion and behavior by anticipating consequences. It may play an important role in delayed gratification by maintaining emotions over time and organizing behavior toward specific goals.[23]
  • Ventral striatum – The ventral striatum is a group of subcortical structures thought to play an important role in emotion and behavior. One part of the ventral striatum called the nucleus accumbens is thought to be involved in the experience of pleasure.[24] Individuals with addictions experience increased activity in this area when they encounter the object of their addiction.
  • Insula – The insular cortex is thought to play a critical role in the bodily experience of emotion, as it is connected to other brain structures that regulate the body's autonomic functions (heart rate, breathing, digestion, etc.). The insula is implicated in empathy and awareness of emotion.[25]
  • Cerebellum – A "Cerebellar Cognitive Affective Syndrome" has been described.[26] Both neuroimaging studies as well as studies following pathological cerebellar lesions (such as a stroke) demonstrate that the cerebellum has a significant role in emotional regulation. Lesion studies[27] have shown that cerebellar dysfunction can attenuate the experience of positive emotions. While these same studies do not show an attenuated response to frightening stimuli, the stimuli did not recruit structures that normally would be activated (such as the amygdala). Rather, alternative structures were activated, such as the ventromedial prefrontal cortex, the anterior cingulate gyrus, and the insula. This may indicate that evolutionary pressure resulted in the development of the cerebellum as a redundant fear-mediating circuit to enhance survival. It may also indicate a regulatory role for the cerebellum in the neural response to rewarding stimuli, such as money,[28] drugs of abuse,[29] and orgasm.[30]
  • Lateral prefrontal cortex
  • Primary sensorimotor cortex
  • Temporal cortex
    • Brainstem

Right hemisphere

The right hemisphere has been proposed as directly involved in emotion processing. Scientific theory regarding its role produced several models of emotional functioning. C. K. Mills was an early researcher who proposed a direct link between the right hemisphere and emotion processing, having observed decreased emotion processing in patients with lesions to the right hemisphere.[31][32] In the late 1980s to early 1990s neocortical structures were shown to have an involvement in emotion.[33] These findings led to the development of the right hemisphere hypothesis and the valence hypothesis.

Right hemisphere hypothesis

The right hemisphere hypothesis asserts that the right hemisphere is specialized for the expression and perception of emotion.[34] It has been linked with mental strategies that are nonverbal, synthetic, integrative, holistic, and gestaltic.[33] The right hemisphere is more in touch with subcortical systems of autonomic arousal and attention as demonstrated in patients that have increased spatial neglect when damage affects the right brain versus the left brain.[35] Right hemisphere pathologies have been linked with abnormal patterns of autonomic nervous system responses.[36] These findings would help signify the strong connection of the subcortical brain regions to the right hemisphere.

Valence hypothesis

The valence hypothesis acknowledges the right hemisphere's role in emotion, but asserts that it is mainly focused on the processing of negative emotions whereas the left hemisphere processes positive emotions. The two hemispheres have been the subject of much debate. One version states that the right hemisphere processes negative emotion leaving positive emotion to the left brain.[37] A second version suggests that the right hemisphere predominates in experiencing both positive and negative emotion.[38][39] More recently, the frontal lobe has been the focus of research, asserting that the frontal lobes of both hemispheres are involved in emotions, while the parietal and temporal lobes are involved in the processing of emotion.[40] Decreased right parietal lobe activity has been associated with depression[41] and increased right parietal lobe activity with anxiety arousal.[42] The increasing understanding of the different hemispheres has led to increasingly complicated models, all based on the original valence model.[43]

Cognitive neuroscience

Despite their interactions, the study of cognition until the late 1990s, excluded emotion and focused on non-emotional processes (e.g., memory, attention, perception, action, problem solving and mental imagery).[44] The study of the neural basis of non-emotional and emotional processes emerged as two separate fields: cognitive neuroscience and affective neuroscience. Emotional and non-emotional processes often involve overlapping neural and mental mechanisms.[45]

Cognitive neuroscience tasks in affective neuroscience research

Emotion go/no-go

The emotion go/no-go task has been used to study behavioral inhibition, particularly emotional modulation of this inhibition.[46] A derivation of the original go/no-go paradigm, this task involves a combination of affective "go cues", where the participant must rapidly make a motor response, and affective "no-go cues", where a response must be withheld. Because "go cues" are more common, the task measures a subject's ability to inhibit a response under different emotional conditions.[47]

The task is common in tests of emotion regulation, and is often paired with neuroimaging measures to localize relevant brain function in both healthy individuals and those with affective disorders.[46][48][49] For example, go/no-go studies converge with other methodology to implicate areas of the prefrontal cortex during inhibition of emotionally valenced stimuli.[50]

Emotional Stroop

The emotional Stroop task, an adaptation to the original Stroop, measures attentional bias to emotional stimuli.[51][52] Participants must name the ink color of presented words while ignoring the words' meanings.[53] In general, participants have more difficulty detaching attention from affectively valenced words, than neutral words.[54][55] This interference from valenced words is measured by the response latency in naming the color of neutral words as compared with emotional words.[52]

This task has been often used to test selective attention to threatening and other negatively valenced stimuli, most often in relation to psychopathology.[56] Disorder-specific attentional biases have been found for a variety of mental disorders.[56][57] For example, participants with spider phobia show a bias to spider-related words but not other negatively valenced words.[58] Similar findings have been attributed to threat words related to other anxiety disorders.[56] However, other studies have questioned these findings. In fact, anxious participants in some studies show the Stroop interference effect for both negative and positive words, when the words are matched for emotionality.[59][60] This means that the specificity effects for various disorders may be largely attributable to the semantic relation of the words to the concerns of the disorder, rather than their emotionality.[56]

Ekman 60 faces task

The Ekman faces task is used to measure emotion recognition of six basic emotions.[61][62] Black and white photographs of 10 actors (6 male, 4 female) are presented, with each actor displaying each emotion. Participants are usually asked to respond quickly with the name of the displayed emotion. The task is a common tool to study deficits in emotion regulation in patients with dementia, Parkinson's, and other cognitively degenerative disorders.[63] The task has been used to analyze recognition errors in disorders such as borderline personality disorder, schizophrenia, and bipolar disorder.[64][65][66]

Dot probe (emotion)

The emotional dot-probe paradigm is a task used to assess selective visual attention to and failure to detach attention from affective stimuli.[67][68] The paradigm begins with a fixation cross at the center of a screen. An emotional stimulus and a neutral stimulus appear side by side, after which a dot appears behind either the neutral stimulus (incongruent condition) or the affective stimulus (congruent condition). Participants are asked to indicate when they see this dot, and response latency is measured. Dots that appear on the same side of the screen as the image the participant was looking at will be identified more quickly. Thus, it is possible to discern which object the participant was attending to by subtracting the reaction time to respond to congruent versus incongruent trials.[67]

The best documented research with the dot probe paradigm involves attention to threat related stimuli, such as fearful faces, in individuals with anxiety disorders. Anxious individuals tend to respond more quickly to congruent trials, which may indicate vigilance to threat and/or failure to detach attention from threatening stimuli.[67][69] A specificity effect of attention has also been noted, with individuals attending selectively to threats related to their particular disorder. For example, those with social phobia selectively attend to social threats but not physical threats.[70] However, this specificity may be even more nuanced. Participants with obsessive-compulsive disorder symptoms initially show attentional bias to compulsive threat, but this bias is attenuated in later trials due to habituation to the threat stimuli.[71]

Fear potentiated startle

Fear-potentiated startle (FPS) has been utilized as a psychophysiological index of fear reaction in both animals and humans.[72] FPS is most often assessed through the magnitude of the eyeblink startle reflex, which can be measured by electromyography.[73] This eyeblink reflex is an automatic defensive reaction to an abrupt elicitor, making it an objective indicator of fear.[74] Typical FPS paradigms involve bursts of noise or abrupt flashes of light transmitted while an individual attends to a set of stimuli.[74] Startle reflexes have been shown to be modulated by emotion. For example, healthy participants tend to show enhanced startle responses while viewing negatively valenced images and attenuated startle while viewing positively valenced images, as compared with neutral images.[75][76]

The startle response to a particular stimulus is greater under conditions of threat.[77] A common example given to indicate this phenomenon is that one's startle response to a flash of light will be greater when walking in a dangerous neighborhood at night than it would under safer conditions. In laboratory studies, the threat of receiving shock is enough to potentiate startle, even without any actual shock.[78]

Fear potentiated startle paradigms are often used to study fear learning and extinction in individuals with post-traumatic stress disorder (PTSD) and other anxiety disorders.[79][80][81] In fear conditioning studies, an initially neutral stimulus is repeatedly paired with an aversive one, borrowing from classical conditioning.[82] FPS studies have demonstrated that PTSD patients have enhanced startle responses during both danger cues and neutral/safety cues as compared with healthy participants.[82][83]

Learning

Affect plays many roles during learning. Deep, emotional attachment to a subject area allows a deeper understanding of the material and therefore, learning occurs and lasts.[84] The emotions evoked when reading in comparison to the emotions portrayed in the content affects comprehension. Someone who is feeling sad understands a sad passage better than someone feeling happy.[85] Therefore, a student's emotion plays an important role during the learning process.

Emotion can be embodied or perceived from words read on a page or in a facial expression. Neuroimaging studies using fMRI have demonstrated that the same area of the brain that is activated when feeling disgust is activated when observing another's disgust.[86] In a traditional learning environment, the teacher's facial expression can play a critical role in language acquisition. Showing a fearful facial expression when reading passages that contain fearful tones facilitates students learning of the meaning of certain vocabulary words and comprehension of the passage.[87]

Models

The neurobiological basis of emotion is still disputed.[2] The existence of basic emotions and their defining attributes represents a long lasting and yet unsettled issue in psychology.[2] The available research suggests that the neurobiological existence of basic emotions is still tenable and heuristically seminal, pending some reformulation.[2]

Basic Emotions

These approaches hypothesize that emotion categories (including happiness, sadness, fear, anger, and disgust) are biologically basic.[88][89] In this view, emotions are inherited, biologically based modules that cannot be separated into more basic psychological components.[88][89][90] Models following this approach hypothesize that all mental states belonging to a single emotional category can be consistently and specifically localized to either a single brain region or a defined network of brain regions.[89][91] Each basic emotion category also shares other universal characteristics: distinct facial behavior, physiology, subjective experience and accompanying thoughts and memories.[88]

Psychological constructionist approaches

This approach to emotion hypothesizes that emotions like happiness, sadness, fear, anger and disgust (and many others) are constructed mental states that occur when brain systems work together.[92] In this view, networks of brain regions underlie psychological operations (e.g., language, attention, etc.) that interact to produce emotion, perception, and cognition.[93] One psychological operation critical for emotion is the network of brain regions that underlie valence (feeling pleasant/unpleasant) and arousal (feeling activated and energized).[92] Emotions emerge when neural systems underlying different psychological operations interact (not just those involved in valence and arousal), producing distributed patterns of activation across the brain. Because emotions emerge from more basic components, heterogeneity affects each emotion category; for example, a person can experience many different kinds of fear, which feel differently, and which correspond to different neural patterns in the brain.

Meta-analyses

A meta-analysis is a statistical approach to synthesizing results across multiple studies. Included studies investigated healthy, unmedicated adults and that used subtraction analysis to examine brain areas that were more active during emotional processing than during a neutral (control) condition.

Phan et al. 2002

In the first neuroimaging meta-analysis of emotion, Phan et al. (2002) analyzed the results of 55 peer reviewed studies between January 1990 and December 2000 to determine if the emotions of fear, sadness, disgust, anger, and happiness were consistently associated with activity in specific brain regions. All studies used fMRI or PET techniques to investigate higher-order mental processing of emotion (studies of low-order sensory or motor processes were excluded). The authors’ tabulated the number of studies that reported activation in specific brain regions. For each brain region, statistical chi-squared analysis was conducted. Two regions showed a statistically significant association. In the amygdala, 66% of studies inducing fear reported activity in this region, as compared to ~20% of studies inducing happiness, ~15% of studies inducing sadness (with no reported activations for anger or disgust). In the subcallosal cingulate, 46% of studies inducing sadness reported activity in this region, as compared to ~20% inducing happiness and ~20% inducing anger. This pattern of clear discriminability between emotion categories was in fact rare, with other patterns occurring in limbic regions, paralimbic regions, and uni/heteromodal regions. Brain regions implicated across discrete emotion included the basal ganglia (~60% of studies inducing happiness and ~60% of studies inducing disgust reported activity in this region) and medial prefrontal cortex (happiness ~60%, anger ~55%, sadness ~40%, disgust ~40%, and fear ~30%).[94]

Murphy et al. 2003

Murphy, et al. 2003 analyzed 106 peer reviewed studies published between January 1994 and December 2001 to examine the evidence for regional specialization of discrete emotions (fear, disgust, anger, happiness and sadness) across a larger set of studies. Studies included in the meta-analysis measured activity in the whole brain and regions of interest (activity in individual regions of particular interest to the study). 3-D Kolmogorov-Smirnov (KS3) statistics were used to compare rough spatial distributions of 3-D activation patterns to determine if statistically significant activations were specific to particular brain regions for all emotional categories. This pattern of consistently activated, regionally specific activations was identified in four brain regions: amygdala with fear (~40% of studies), insula with disgust (~70%), globus pallidus with disgust (~70%), and lateral orbitofrontal cortex with anger (80%). Other regions showed different patterns of activation across categories. For example, both the dorsal medial prefrontal cortex and the rostral anterior cingulate cortex showed consistent activity across emotions (happiness ~50%, sadness ~50%, anger ~ 40%, fear ~30%, and disgust ~ 20%).[95]

Barrett et al. 2006

Barrett, et al. 2006 examined 161 studies published between 1990 and 2001. The authors compared the consistency and specificity of prior meta-analytic findings specific to each notional basic emotion. Consistent neural patterns were defined by brain regions showing increased activity for a specific emotion (relative to a neutral control condition), regardless of the method of induction used (for example, visual vs. auditory cue). Specific neural patterns were defined as separate circuits for one emotion vs. the other emotions (for example, the fear circuit must be discriminable from the anger circuit, although both may include common brain regions). In general, the results supported Phan et al. and Murphy et al., but not specificity. Consistency was determined through the comparison of chi-squared analyses that revealed whether the proportion of studies reporting activation during one emotion was significantly higher than the proportion of studies reporting activation during the other emotions. Specificity was determined through the comparison of emotion-category brain-localizations by contrasting activations in key regions that were specific to particular emotions. Increased amygdala activation during fear was the most consistently reported across induction methods (but not specific). Both meta-analyses associated the anterior cingulate cortex with sadness, although this finding was less consistent (across induction methods) and was not specific. Both meta-analyses found that disgust was associated with the basal ganglia, but these findings were neither consistent nor specific. Neither consistent nor specific activity was observed across the meta-analyses for anger or happiness. This meta-analysis introduced the concept of the basic, irreducible elements of emotional life as dimensions such as approach and avoidance.[92]

Kober et al. 2008

Kober, et al. 2008 reviewed 162 neuroimaging studies published between 1990–2005 to determine if groups of brain regions showed consistent activation patterns while experiencing an emotion directly and (indirectly) as experienced by another. This analysis used multilevel kernel density analysis (MKDA) to examine fMRI and PET studies, a technique that prevents single studies from dominating the results (particularly if they report multiple nearby peaks) and that enables studies involving more participants to exert more influence upon the results. MKDA was used to establish a neural reference space that includes the set of regions showing consistent increases across all studies.[96] This neural reference space was partitioned into functional groups of brain regions showing similar activation patterns by using multivariate techniques to determine co-activation patterns and then using data-reduction techniques to define the functional groupings, resulting in six groups. The authors discussed each functional group in terms of more basic psychological operations.

Groups
Group Regions Notes
Core limbic left amygdala, hypothalamus, periaqueductal gray/thalamus regions, and amygdala/ventral striatum/ventral globus pallidus/thalamus regions Integrative emotional center that plays a general role in evaluating affective significance.
Lateral Paralimbic ventral anterior insula/frontal operculum/right temporal pole/ posterior orbitofrontal cortex, the anterior insula/ posterior orbitofrontal cortex, the ventral anterior insula/ temporal cortex/ orbitofrontal cortex junction, the midinsula/ dorsal putamen, and the ventral striatum /mid insula/ left hippocampus Plays a role in motivation, contributing to the general valuation of stimuli and particularly in reward.
Medial Prefrontal Cortex dorsal medial prefrontal cortex, pregenual anterior cingulate cortex, and rostral dorsal anterior cingulate cortex Plays a role in both the generation and regulation of emotion.
Cognitive/ Motor Network right frontal operculum, the right interior frontal gyrus, and the pre-supplementray motor area/ left interior frontal gyrus, regions Not specific to emotion, but instead appear to play a more general role in information processing and cognitive control.
Occipital/ Visual Association V8 and V4 areas of the primary visual cortex, the medial temporal lobe, and the lateral occipital cortex
Medial Posterior posterior cingulate cortex and area V1 of the primary visual cortex

The authors suggest that these regions play a joint role in visual processing and attention to emotional stimuli.[97]

Vytal et al. 2010

Vytal, et al. 2010 examined 83 neuroimaging studies published between 1993–2008 to examine whether neuroimaging evidence supports biologically discrete, basic emotions (i.e. fear, anger, disgust, happiness, and sadness). Consistency analyses identified brain regions associated with individual emotions. Discriminability analyses identified brain regions that were differentially active under contrasting pairs of emotions. This meta-analysis examined PET or fMRI studies that reported whole brain analyses identifying significant activations for at least one of the five emotions relative to a neutral or control condition. The authors used activation likelihood estimation (ALE) to perform spatially sensitive, voxel-wise (sensitive to the spatial properties of voxels) statistical comparisons across studies. This technique allows for direct statistical comparison between activation maps associated with each discrete emotion. Thus, discriminability between the five discrete emotion categories was assessed on a more precise spatial scale than in prior meta-analyses.

Consistency was first assessed by comparing the cross-study ALE map for each emotion to ALE maps generated by random permutations. Discriminability was assessed by pair-wise contrasts of emotion maps. Consistent and discriminable activation patterns were observed for the five categories.

Associations[98]
Emotion Peak Regions
Happiness right superior temporal gyrus, left rostral anterior cingulate cortex 9 regional brain clusters
Sadness left medial frontal gyrus 35 clusters - especially, left medial frontal gyrus, right middle temporal gyrus, and right inferior frontal gyrus
Anger left inferior frontal gyrus 13 clusters - bilateral inferior frontal gyrus, and in right parahippocampal gyrus
Fear left amygdala 11 clusters - left amygdala and left putamen
Disgust right insula/ right inferior frontal gyrus 16 clusters - right putamen and the left insula.

Lindquist et al. 2012

Lindquist, et al. reviewed 91 PET and fMRI studies published between January 1990 and December 2007. The studies used induction methods that elicit emotion experience or emotion perception of fear, sadness, disgust, anger, and happiness. The goal was to compare basic emotions approaches with psychological constructionist approaches. A MKDA[96] transformed the individual peak into a neural reference space. The density analysis was then used to identify voxels with more consistent activations for a specific emotion category than all other emotions. Chi-squared analysis was used to create statistical maps that indicated whether each previously identified and consistently active region was more frequently activated in studies of each emotion category than average, regardless of activations elsewhere in the brain. Chi-squared analysis and density analysis both defined functionally consistent and selective regions (regions that showed a more consistent activity increase) for one emotion category. Thus, a selective region could present increased activations to multiple emotions, as long as the response to one emotion was relatively stronger.

A series of logistic regressions were performed to identify regions that while consistent and selective to an emotion were additionally specific to that emotion. Specificity was defined as showing increased activations for only one emotional category. Strong support for basic emotions was defined as evidence that brain areas respond to only one emotional category. Strong support for the constructionist approach was defined as evidence that psychological operations consistently occur across many brain regions and multiple emotional categories.

The results indicated that many brain regions demonstrated consistent and selective activations in the experience or perception of one emotion category. Consistent with constructionist models, however, no region demonstrated functional specificity for the emotions of fear, disgust, happiness, sadness or anger.

The authors proposed different roles for the brain regions that have traditionally been associated with only one emotion category. The authors propose that the amygdala, anterior insula, orbitofrontal cortex each contribute to "core affect", which are basic feelings that are pleasant or unpleasant with some level of arousal.

Core affects
Region Role
Amygdala indicating whether external sensory information is motivationally salient, novel and/oor evokes uncertainty
Anterior insula represents core affective feelings in awareness across emotion categories, driven largely by body sensations
Orbitofrontal cortex functions as a site for integrating sensory information from the body and the world to guide behavior

Closely related to core affect, the authors propose that the anterior cingulate and dorsolateral prefrontal cortex play vital roles in attention. The anterior cingulate supports the use of sensory information for directing attention and motor responses during response selection while the dorsolateral prefrontal cortex supporting executive attention. In many psychological construction approaches, emotions relate an individual's situation in the world to internal body states, referred to as "conceptualization". The dorsomedial prefrontal cortex and hippocampus were consistently active in this context: regions that play an important role conceptualizing are also involved in simulating previous experience (e.g. knowledge, memory). Language is also central to conceptualizing, and regions that support language, including ventrolateral prefrontal cortex, were also consistently active across studies of emotion experience and perception.[93]

See also

References

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  2. ↑ 2.0 2.1 2.2 2.3 Celeghin, Alessia; Diano, Matteo; Bagnis, Arianna; Viola, Marco; Tamietto, Marco (2017). "Basic Emotions in Human Neuroscience: Neuroimaging and Beyond". Frontiers in Psychology 8: 1432. doi:10.3389/fpsyg.2017.01432. ISSN 1664-1078. PMID 28883803.  This article incorporates text by Alessia Celeghin, Matteo Diano, Arianna Bagnis, Marco Viola, and Marco Tamietto available under the CC BY 4.0 license.
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  13. ↑ Modi, Shilpi; R. Trivedi; K. Singh; P. Kumar; R. Rathore; R. Tripathi; S. Khushu (2012). "Individual differences in trait anxiety are associated with white matter tract integrity in fornix and uncinate fascicles: Preliminary evidence from a DTI based tractography study". Behavioural Brain Research 238: 188–192. doi:10.1016/j.bbr.2012.10.007. PMID 23085341. 
  14. ↑ Seralynne D. Vann (2010). "Re-evaluating the role of the mammillary bodies in memory". Neuropsychologia 48 (8): 2316–2327. doi:10.1016/j.neuropsychologia.2009.10.019. PMID 19879886. http://psych.cf.ac.uk/home2/vann/VannNeuro2010.pdf. 
  15. ↑ "olfactory bulb". http://www.sci.uidaho.edu/med532/olfacbulb.htm. 
  16. ↑ "Cingulate Gyrus: Functional Correlations of the 4 Cingulate Regions". Cingulum NeuroSciences Institute.. http://www.cingulumneurosciences.org/functional.shtml. 
  17. ↑ D.H. Weissman; A. Gopalakrishnan; C.J. Hazlett; M.G. Woldorff (2005). "Dorsal Anterior Cingulate Cortex Resolves Conflict from Distracting Stimuli by Boosting Attention toward Relevant Events". Cerebral Cortex 15 (2): 229–237. doi:10.1093/cercor/bhh125. PMID 15238434. 
  18. ↑ 18.0 18.1 Medford N; Critchley HD. (June 2010). "Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response". Brain Struct Funct 214 (5–6): 535–549. doi:10.1007/s00429-010-0265-x. PMID 20512367. 
  19. ↑ Drevets, Wayne C.; Savitz, Jonathan; Trimble, Michael (15 December 2016). "The Subgenual Anterior Cingulate Cortex in Mood Disorders". CNS Spectrums 13 (8): 663–681. doi:10.1017/s1092852900013754. ISSN 1092-8529. PMID 18704022. 
  20. ↑ Da Cunha C; Gomez-A A; Blaha CD. (2012). "The role of the basal ganglia in motivated behavior". Rev Neurosci. 23 (5–6): 747–67. doi:10.1515/revneuro-2012-0063. PMID 23079510. 
  21. ↑ Mikhael, John G.; Bogacz, Rafal (2 September 2016). "Learning Reward Uncertainty in the Basal Ganglia". PLOS Computational Biology 12 (9): e1005062. doi:10.1371/journal.pcbi.1005062. ISSN 1553-7358. PMID 27589489. Bibcode: 2016PLSCB..12E5062M. 
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  23. ↑ Davidson, R.J.; Sutton, S.K. (1995). "Affective neuroscience: The emergence of a discipline". Current Opinion in Neurobiology 5 (2): 217–224. doi:10.1016/0959-4388(95)80029-8. PMID 7620310. 
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Further reading

  • Davidson, R.J.; Irwin, W. (1999). "The functional neuroanatomy of emotion and affective style". Trends in Cognitive Sciences 3 (1): 11–21. doi:10.1016/s1364-6613(98)01265-0. PMID 10234222. 
  • Panksepp, J. (1992). "A critical role for affective neuroscience in resolving what is basic about basic emotions". Psychological Review 99 (3): 554–60. doi:10.1037/0033-295x.99.3.554. PMID 1502276. 
  • Harmon-Jones E, & Winkielman P. (Eds.) Social Neuroscience: Integrating Biological and Psychological Explanations of Social Behavior. New York: Guilford Publications.
  • Cacioppo, J.T., & Berntson, G.G. (2005). Social Neuroscience. Psychology Press.
  • Cacioppo, J.T., Tassinary, L.G., & Berntson, G.G. (2007). Handbook of Psychophysiology. Cambridge University Press.
  • Panksepp J. (1998). Affective Neuroscience: The Foundations of Human and Animal Emotions (Series in Affective Science). Oxford University Press, New York, New York.
  • Brain and Cognition, Vol. 52, No. 1, pp. 1–133 (June, 2003). Special Issue on Affective Neuroscience.




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