The bivalent side of the nucleus accumbens
Section snippets
Subjects
Twenty right-handed adults (10 male, 10 female; age: range 20–31, mean 25.7 ± 0.6; IQ = 116 ± 2.7) took part in the study. Subjects were free of any medical or neurological problems, and had no current or previous diagnosis of psychiatric or neurological disorder. All subjects gave informed consent in accordance with Weill Medical College of Cornell University IRB committee, and were paid for their participation.
Stimuli and apparatus
Auditory stimuli consisting of two unpleasant (negative tones: n1 and n2) and two
Validation of stimulus valence
At the end of the experimental session, while still in the scanner, subjects rated the auditory stimuli presented with respect to their positive and negative stimulus valence. There was a significant difference in valence ratings between the positive and negative stimuli presented (Fig. 1B), where positive sounds were rated as pleasant and negative sounds were rated as unpleasant (Z = − 3.9, p ≤ 0.001). No gender differences were found in valence rating, nor did valence ratings differ with respect
Discussion
We found that the NAcc responds to the onset of both positive and negative stimuli. Onset and offset analysis of activation of the NAcc to pleasant and unpleasant sounds in a passive listening paradigm confirmed a direct activation of this region by aversive stimuli, rather than an effect secondary to some kind of relief, or a result of preparation and regulation of instrumental motor action. These results support the expanded view of NAcc function, whereby the NAcc plays a key role in
Acknowledgments
We would like to thank Bruce McCandliss and Jason Zevin for their thoughtful discussions about this work. This research was supported in part by the National Institute of Drug Abuse Grant R01 DA018879 (BJC), NIH P50 MH52196 and MH079513, the Mortimer D. Sackler family and Dewitt-Wallace Reader's Digest Foundation.
References (91)
- et al.
Reward circuitry activation by noxious thermal stimuli
Neuron
(2001) - et al.
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Neuron
(2007) - et al.
Dopamine functions in appetitive and defensive behaviours
Prog. Neurobiol.
(1992) - et al.
A network representation of response probability in the striatum
Neuron
(2002) - et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Acute and subacute effects of risperidone and cocaine on accumbens dopamine and serotonin release using in vivo microvoltammetry on line with open-field behavior
Prog. Neuropsychopharmacol. Biol. Psychiatry
(2003) - et al.
Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex
Neurosci. Biobehav. Rev.
(2002) - et al.
Neurobiological regret and rejoice functions for aversive outcomes
NeuroImage
(2008) - et al.
Valence and salience contribute to nucleus accumbens activation
NeuroImage
(2008) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages
Comput. Biomed. Res.
(1996)
Extending animal models of fear conditioning to humans
Biol. Psychol.
Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces
Neuron
Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain
Neuron
Gating of information flow within the limbic system and the pathophysiology of schizophrenia
Brain Res. Brain Res. Rev.
An electrophysiological characterization of ventral tegmental area dopaminergic neurons during differential Pavlovian fear conditioning in the awake rabbit
Behav. Brain Res.
Accumbens dopamine–acetylcholine balance in approach and avoidance
Curr. Opin. Pharmacol.
Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events
Neuroscience
Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum
Behav. Brain Res.
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Brain Res. Brain Res. Rev.
Direct activation of the ventral striatum in anticipation of aversive stimuli
Neuron
Brain regions associated with the expression and contextual regulation of anxiety in primates
Biol. Psychiatry
Topographical organization in the nucleus accumbens of afferents from the basolateral amygdala and efferents to the lateral hypothalamus
Neuroscience
AP-7 into the nucleus accumbens disrupts acquisition but does not affect consolidation in a passive avoidance task
Physiol. Behav.
Mesencephalic dopaminergic unit activity in the behaviorally conditioned rat
Life Sci.
Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning
NeuroImage
Extinction learning in humans: role of the amygdala and vmPFC
Neuron
Contributions of the amygdala to emotion processing: from animal models to human behavior
Neuron
Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli
Brain Res.
Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output
Neuron
Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine
Curr. Opin. Pharmacol.
Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis
Neurosci. Biobehav. Rev.
Dopamine neurons and their role in reward mechanisms
Curr. Opin. Neurobiol.
Temporary inactivation of the nucleus accumbens disrupts acquisition and expression of fear-potentiated startle in rats
Brain Res.
Neural encoding in ventral striatum during olfactory discrimination learning
Neuron
Waiting for spiders: brain activation during anticipatory anxiety in spider phobics
NeuroImage
The nucleus accumbens: a target for deep brain stimulation in obsessive–compulsive- and anxiety-disorders
J. Chem. Neuroanat.
Suppression of conditioned avoidance behavior by the local application of (−)sulpiride into the ventral, but not the dorsal, striatum of the rat
Biol. Psychiatry
The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division
Biol. Psychiatry
Behavioral and electrophysiological indices of negative affect predict cocaine self-administration
Neuron
Neuronal responses in the ventral striatum of the behaving macaque
Behav. Brain Res.
The nucleus accumbens unit activities related to the emotional significance of complex environmental stimuli in freely moving cats
Neurosci. Res.
Human striatal activation reflects degree of stimulus saliency
NeuroImage
Fear conditioning in C57/BL/6 and DBA/2 mice: variability in nucleus accumbens function according to the strain predisposition to show contextual- or cue-based responding
Eur. J. Neurosci.
Parabrachial internal lateral neurons convey nociceptive messages from the deep laminas of the dorsal horn to the intralaminar thalamus
J. Neurosci.
Limbic corticostriatal systems and delayed reinforcement
Ann. N. Y. Acad. Sci.
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2021, Behavioural Brain ResearchCitation Excerpt :The PPE_low group mainly felt disgusted while watching the PP videos, which was accompanied by NAc deactivation. Although the NAc is often described as one part of the ‘pleasure system’ of the brain (for a review see [18]), this region is also involved in modulating responses to aversive events (e.g., [19–22]). For example, Becerra et al. [19] showed that pain onset (aversion) resulted in a negative activity change in the NAc, while pain offset (relief) produced a positive activity change.