ReviewNeurobiology of emotion perception I: the neural basis of normal emotion perception
Introduction
Critical to survival is the ability to identify quickly in the environment emotionally salient information, including danger and reward, and to form rapid and appropriate behavioral responses (Darwin 1872/1965). Although it is clear that the presence of an emotion involves physiologic arousal, appraisal, subjective experience, expression, and goal-directed behavior (Plutchik 1984), there is at present no generally accepted theoretical framework for human emotion and limited understanding of the neurobiological basis of the different processes underlying emotion perception. In this critical review, by examining the findings from recent animal, human lesion, and functional neuroimaging studies, we have aimed to identify the neural basis of a series of different neuropsychological processes important to the understanding of normal human emotional behavior.
Section snippets
Neuropsychological processes underlying emotion perception
Early theories proposed to explain the neuropsychological basis of emotion perception Cannon 1929, James 1884 emphasized the importance of feedback from bodily responses to an emotionally salient stimulus in determining the nature and extent of emotional feeling, but they did not distinguish between the identification of the emotive stimulus and the affective state produced in response to this. Appraisalist theories of emotion Arnold 1960, Lazarus 1991, and current researchers (Clore and Ortony
Animal studies
Many of these studies have been helpful in determining neural regions associated with behavioral responses to emotive stimuli (i.e., the combination of processes 1 and 2), whereas other studies have attempted to examine regions associated predominantly with process 1. These have demonstrated the importance of the amygdala in the initial response to emotionally salient stimuli. Cells in the amygdala responding selectively to faces and eye gaze direction have been identified in studies of
Animal studies
The existence of brain regions specialized for reward processing was initially suggested by studies showing that rats responded operantly to stimulation of specific sites to the exclusion of other activities (Olds and Milner 1954). These included the midbrain dopaminergic projections from the ventral tegmental area into the nucleus accumbens shell region and the medial prefrontal cortex (Spanagel and Weiss 1999). In primates, regions important for reward processing have been identified as the
Animal studies
Studies have implicated the medial prefrontal cortex in the regulation of affective state and emotional behavior (Mega et al 1997). This region is strategically located between two broad trends or compartments in cortical evolution (Sanides 1970). The ventrolateral trend is reactive-based, operates by feedback, and is derived from archicortex (olfactory cortex). In addition to the response to emotional stimuli, ventral prefrontal regions appear to have a role in emotional behavioral regulation
Conclusions: neural systems for emotion perception
In this review, we have described findings from studies employing a variety of techniques and specific experimental paradigms, which have helped to increase understanding of the neural basis of neuropsychological processes important for emotion perception, namely: the identification of the emotional significance of an environmental stimulus; the production of an affective state and emotional behavior; and the regulation of the affective state and emotional behavior, allowing the generation of
References (144)
- et al.
Autonomic and somatomotor effects of amygdala central nucleus stimulation in awake rabbits
Psychol Behav
(1983) Circuitry and functional aspects of the insular lobe in primates including humans
Brain Res Rev
(1996)- et al.
The GSR of monkeys during orienting and habituation and after ablation of the amygdala, hippocampus and inferotemporal cortex
Neuropsychologia
(1965) - et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Acute effects of cocaine on human brain activity and emotion
Neuron
(1997) - et al.
Mesial temporal neurons in the macaque monkey with responses selective for aspects of social stimuli
Behav Brain Res
(1993) - et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends Cognit Sci
(2000) - et al.
Psychosurgery
Neurosurg Clin North Am
(1995) - et al.
Neural activity in the human brain relating to uncertainty and arousal during anticipation
Neuron
(2001) - et al.
Anger in healthy menA PET study using script-driven imagery
Biol Psychiatry
(1999)
Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria
Biol Psychiatry
Effect of familiarity on the processing of human faces
Neuroimage
The effect of medial frontal cortex lesions on cardiovascular conditioned emotional responses in the rat
Brain Res
Error potentials in limbic cortex (anterior cingulate area 24) of monkeys during motor learning
Neurosci Lett
Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage
Neuropsychologia
Effects of early adverse experiences on brain structure and functionClinical implications
Biol Psychiatry
Regional brain activity during transient self-induced anxiety and anger in healthy adults
Biol Psychiatry
Human amygdala activation during conditioned fear acquisition and extinctionA mixed-trial fMRI study
Neuron
Task instructions modulate neural responses to fearful facial expressions
Biol Psychiatry
Bilateral infarction of the anterior cingulate gyri and of the fornices. Report of a case
J Neurol Sc
Childhood obsessive-compulsive disorder and cingulate epilepsy
Biol Psychiatry
Role of midline frontolimbic cortex in production of the isolation call of squirrel monkeys
Brain Res
Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys
Neuropsychologia
Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats
Neurobiol Learn Mem
Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala
Nature
Episodic memory, amnesia and the hippocamal-anterior thalamic axis
Behav Brain Sci
Basal ganglia-thalamocortical circuitsParallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions
Prog Brain Re
Lesions of the human amygdala impair enhanced perception of emotionally salient events
Nature
Focal lesion of the right cingulumA case report in a child
J Neurol Neurosurg Psychiatry
Emotion and Personality
Clinical semiology of frontal lobe seizures
Adv Neurol
The neural basis of romantic love
Neuroreport
Neural correlates of conscious self-regulation of emotion
J Neurosci
Dissociation of working memory from decision making within the human prefrontal cortex
J Neurosci
Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans
Science
Dissociable neural responses to facial expressions of sadness and anger
Brain
Innate and conditioned reactions to threat in rats with amygdaloid lesions
J Comp Physiol Psychol
Conflict monitoring versus selection-for-action in anterior cingulate cortex
Nature
Cingulothalamic and prefrontal control of autonomic function
Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging
J Neurosci
Amygdala activity at encoding correlated with long-term, free recall of emotional information
Proc Natl Acad Sci U S A
Neuropsychology of fear and loathing
Nat Rev Neurosci
Event-related activation in the human amygdala associates with later memory for individual emotional experiences
J Neurosci
Anterior cingulate cortex, error detection, and on-line monitoring of performance
Science
Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli
J Neurophysiol
Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain
J Neurophysiol
The neurobiological basis of anxiety disorders
Cognition in emotionAlways, sometimes or never
Brain activity during biofeedback relaxation. A functional neuroimaging investigation
Brain
Cited by (1763)
The relationship between alexithymia, rumination and binge drinking among university students
2024, Personality and Individual DifferencesAbnormal functional connectivity of the intrinsic networks in adolescent bipolar I versus bipolar II disorder
2024, Psychiatry Research - NeuroimagingGray matter morphological abnormities are constrained by normal structural covariance network in OCD
2024, Progress in Neuro-Psychopharmacology and Biological PsychiatryTowards the neurobiology of insomnia: A systematic review of neuroimaging studies
2024, Sleep Medicine ReviewsShared and Distinct Neurobiological Bases of Bipolar Disorder and Attention-Deficit/Hyperactivity Disorder in Children and Adolescents: A Comparative Meta-analysis of Structural Abnormalities
2024, Journal of the American Academy of Child and Adolescent Psychiatry