Abstract
Background
The developmental trajectory of psychopathy seemingly begins early in life and includes
the presence of callous-unemotional (CU) traits (e.g., deficient emotional reactivity,
callousness) in conduct-disordered (CD) youth. Though subregion-specific anomalies
in amygdala function have been suggested in CU pathophysiology among antisocial populations,
system-level studies of CU traits have typically examined the amygdala as a unitary
structure. Hence, nothing is yet known of how amygdala subregional network function
may contribute to callous-unemotionality in severely antisocial people.
Methods
We addressed this important issue by uniquely examining the intrinsic functional connectivity
of basolateral amygdala (BLA) and centromedial amygdala (CMA) networks across three
matched groups of juveniles: CD offenders with CU traits (CD/CU+; n = 25), CD offenders without CU traits (CD/CU−; n = 25), and healthy control subjects (n = 24). We additionally examined whether perturbed amygdala subregional connectivity
coincides with altered volume and shape of the amygdaloid complex.
Results
Relative to CD/CU− and healthy control youths, CD/CU+ youths showed abnormally increased
BLA connectivity with a cluster that included both dorsal and ventral portions of
the anterior cingulate and medial prefrontal cortices, along with posterior cingulate,
sensory associative, and striatal regions. In contrast, compared with CD/CU− and healthy
control youths, CD/CU+ youths showed diminished CMA connectivity with ventromedial/orbitofrontal
regions. Critically, these connectivity changes coincided with local hypotrophy of
BLA and CMA subregions (without being statistically correlated) and were associated
to more severe CU symptoms.
Conclusions
These findings provide unique insights into a putative mechanism for perturbed attention-emotion
interactions, which could bias salience processing and associative learning in youth
with CD/CU+.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological PsychiatryAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Antisocial behavior from a developmental psychopathology perspective.Dev Psychopathol. 2009; 21: 1111-1131
- Psychopathy: Developmental perspectives and their implications for treatment.Restor Neurol Neurosci. 2014; 32: 103-117
- The psychopath magnetized: Insights from brain imaging.Trends Cogn Sci. 2012; 16: 52-60
- The neurobiology of psychopathic traits in youths.Nat Rev Neurosci. 2013; 14: 786-799
- Functional connectivity bias in the prefrontal cortex of psychopaths.Biol Psychiatry. 2015; 78: 647-655
- Reduced prefrontal connectivity in psychopathy.J Neurosci. 2011; 31: 17348-17357
- Amygdala subnuclei connectivity in response to violence reveals unique influences of individual differences in psychopathic traits in a nonforensic sample.Hum Brain Mapp. 2015; 36: 1417-1428
- Reduced amygdala-orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits.Psychiatry Res. 2011; 194: 279-286
- An fMRI study of affective perspective taking in individuals with psychopathy: Imagining another in pain does not evoke empathy.Front Hum Neurosci. 2013; 7: 489
- Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits.Psychiatry Res. 2012; 202: 239-244
- A model of differential amygdala activation in psychopathy.Psychol Rev. 2012; 119: 789-806
- The amygdala.Curr Biol. 2007; 17: R868-R874
- The amygdaloid complex: Anatomy and physiology.Physiol Rev. 2003; 83: 803-834
- Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey.Neuroscience. 2002; 115: 1261-1279
- Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging.Nat Rev Neurosci. 2007; 8: 700-711
- Functional connectivity of the human amygdala using resting state fMRI.Neuroimage. 2009; 45: 614-626
- The development of human amygdala functional connectivity at rest from 4 to 23 years: A cross-sectional study.Neuroimage. 2014; 95: 193-207
- Immature integration and segregation of emotion-related brain circuitry in young children.Proc Natl Acad Sci U S A. 2012; 109: 7941-7946
- Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder.J Am Acad Child Adolesc Psychiatry. 2013; 52 (.e2): 290-299
- Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder.Arch Gen Psychiatry. 2009; 66: 1361-1372
- Abnormal functional architecture of amygdala-centered networks in adolescent posttraumatic stress disorder.Hum Brain Mapp. 2016; 37: 1120-1135
- Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood.Biol Psychiatry. 2014; 75: 892-900
- Plasticity in gray and white: neuroimaging changes in brain structure during learning.Nat Neurosci. 2012; 15: 528-536
- Morphological alterations in the prefrontal cortex and the amygdala in unsuccessful psychopaths.J Abnorm Psychol. 2010; 119: 546-554
- Localization of deformations within the amygdala in individuals with psychopathy.Arch Gen Psychiatry. 2009; 66: 986-994
- Schedule for Affective Disorders and Schizophrenia for School-Age Children Present and Lifetime version (K-SADS-PL): Initial reliability and validity data.J Am Acad Child Adolesc Psychiatry. 1997; 36: 980-988
- Neural responses to fearful eyes in children with conduct problems and varying levels of callous-unemotional traits.Psychol Med. 2014; 44: 99-109
- Amygdala response to preattentive masked fear in children with conduct problems: The role of callous-unemotional traits.Am J Psychiatry. 2012; 169: 1109-1116
- The Inventory of Callous-Unemotional Traits.The University of New Orleans, New Orleans2004
- Associations between high callous-unemotional traits and quality of life across youths with non-conduct disorder diagnoses.Eur Child Adolesc Psychiatry. 2016; 25: 547-555
- Assessing the affective features of psychopathy in adolescence: A further validation of the inventory of callous and unemotional traits.Assessment. 2010; 17: 44-57
- Adolescent callous-unemotional traits and conduct disorder in adoptees exposed to severe early deprivation.Br J Psychiatry. 2012; 200: 197-201
- Assessing callous-unemotional traits in adolescent offenders: Validation of the Inventory of Callous-Unemotional Traits.Int J Law Psychiatry. 2008; 31: 241-252
- Establishing cut-off scores for the parent-reported inventory of callous-unemotional traits.Arch Forensic Psychol. 2014; 1: 27-48
- The Inventory of Callous and Unemotional Traits: A construct-validational analysis in an at-risk sample.Assessment. 2013; 20: 532-544
- Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.Neuroimage. 2012; 59: 2142-2154
- An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data.Neuroimage. 2013; 64: 240-256
- A Bayesian model of shape and appearance for subcortical brain segmentation.Neuroimage. 2011; 56: 907-922
- The role of prefrontal cortex in psychopathy.Rev Neurosci. 2012; 23: 253-262
- Emotional processing in anterior cingulate and medial prefrontal cortex.Trends Cogn Sci. 2011; 15: 85-93
- Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: Disruptions in neurodevelopmental psychiatric disorders.J Am Acad Child Adolesc Psychiatry. 2012; 51: 356-367
- The cross-functional role of frontoparietal regions in cognition: Internal attention as the overarching mechanism.Prog Neurobiol. 2014; 116: 66-86
- Reprint of: Emotion and cognition and the amygdala: From “what is it?” to “what’s to be done?”.Neuropsychologia. 2011; 49: 681-694
- Functional anatomy of ventromedial prefrontal cortex: Implications for mood and anxiety disorders.Mol Psychiatry. 2012; 17: 132-141
- Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices.Brain Res Bull. 2000; 52: 319-330
- Extinction circuits for fear and addiction overlap in prefrontal cortex.Learn Mem. 2009; 16: 279-288
- Neurons in medial prefrontal cortex signal memory for fear extinction.Nature. 2002; 420: 70-74
- Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear.Learn Mem. 2006; 13: 728-733
- Sensory inputs to intercalated cells provide fear-learning modulated inhibition to the basolateral amygdala.Neuron. 2015; 86: 541-554
- From circuits to behaviour in the amygdala.Nature. 2015; 517: 284-292
- Amygdala inhibitory circuits and the control of fear memory.Neuron. 2009; 62: 757-771
- Amygdala microcircuits controlling learned fear.Neuron. 2014; 82: 966-980
- Overlapping neural systems mediating extinction, reversal and regulation of fear.Trends Cogn Sci. 2010; 14: 268-276
- Connections of the medial posterior parietal cortex (area 7m) in the monkey.Anat Rec. 2001; 263: 215-236
- Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus-monkey: Evidence for a distributed neural network subserving spatially guided behavior.J Neurosci. 1988; 8: 4049-4068
- Amygdalo-cortical projections in the monkey (Macaca-fascicularis).J Comp Neurol. 1984; 230: 465-496
- An investigation of the structural, connectional, and functional subspecialization in the human amygdala.Hum Brain Mapp. 2013; 34: 3247-3266
- Structural connectivity of the developing human amygdala.PLoS One. 2015; 10: e0125170
- Psychopathy, attention and emotion.Psychol Med. 2009; 39: 543-555
- The interplay of attention and emotion: Top-down attention modulates amygdala activation in psychopathy.Cogn Affect Behav Neurosci. 2013; 13: 757-770
- Author response: Reactive aggression and functional, not neural, specificity.Br J Psychol. 2010; 101: 407-410
- Psychopathy: Cognitive and neural dysfunction.Dialogues Clin Neurosci. 2013; 15: 181-190
- Psychopathic personality traits associated with abnormal selective attention and impaired cognitive control.Neuropsychology. 2008; 22: 669-680
- Lesions of the basolateral amygdala disrupt conditioning based on the retrieved representations of motivationally significant events.J Neurosci. 2006; 26: 8305-8309
- Amygdala neurons differentially encode motivation and reinforcement.J Neurosci. 2007; 27: 3937-3945
- The potential role of the striatum in antisocial behavior and psychopathy.Biol Psychiatry. 2012; 72: 817-822
- The reward circuit: Linking primate anatomy and human imaging.Neuropsychopharmacology. 2010; 35: 4-26
- Neuroanatomy of reward: A view from the ventral striatum.in: Gottfried J.A. Neurobiology of Sensation and Reward. CRC Press, Boca Raton, FL2011
- The amygdala and basal forebrain as a pathway for motivationally guided attention.J Neurosci. 2014; 34: 13757-13767
- Psychopathic tendencies and mesolimbic recruitment by cues for instrumental and passively obtained rewards.Biol Psychol. 2012; 89: 408-415
- Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits.Nat Neurosci. 2010; 13: 419-421
- Neural correlates of reward and loss sensitivity in psychopathy.Soc Cogn Affect Neurosci. 2014; 9: 794-801
- Disrupted reinforcement signaling in the orbitofrontal cortex and caudate in youths with conduct disorder or oppositional defiant disorder and a high level of psychopathic traits.Am J Psychiatry. 2011; 168: 152-162
- Disrupted expected value and prediction error signaling in youths with disruptive behavior disorders during a passive avoidance task.Am J Psychiatry. 2013; 170: 315-323
- Incentive processing in persistent disruptive behavior and psychopathic traits: A functional magnetic resonance imaging study in adolescents.Biol Psychiatry. 2015; 78: 615-624
- Encoding of conditioned fear in central amygdala inhibitory circuits.Nature. 2010; 468 (277-239)
- The amygdala and medial prefrontal cortex: Partners in the fear circuit.J Physiol. 2013; 591: 2381-2391
- Cortical afferents to the extended amygdala.Ann N Y Acad Sci. 1999; 877: 309-338
- Attention moderates the fearlessness of psychopathic offenders.Biol Psychiatry. 2010; 67: 66-70
- Aberrant paralimbic gray matter in criminal psychopathy.J Abnorm Psychol. 2012; 121: 649-658
- Lower amygdala volume in men is associated with childhood aggression, early psychopathic traits, and future violence.Biol Psychiatry. 2014; 75: 73-80
- Aberrant paralimbic gray matter in incarcerated male adolescents with psychopathic traits.J Am Acad Child Adolesc Psychiatry. 2013; 52 (.e3): 94-103
- Post-training unilateral amygdala lesions selectively impair contextual fear memories.Learn Mem. 2012; 19: 256-263
- The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament.J Neurosci. 2001; 21: 2067-2074
- The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta).Behav Neurosci. 2006; 120: 761-786
- A mechanism for impaired fear recognition after amygdala damage.Nature. 2005; 433: 68-72
- Lesions of the human amygdala impair enhanced perception of emotionally salient events.Nature. 2001; 411: 305-309
- Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe.Neuropsychology. 2001; 15: 30-38
- Stress and the social brain: Behavioural effects and neurobiological mechanisms.Nat Rev Neurosci. 2015; 16: 290-304
- Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals.PLoS One. 2012; 7: e46970
Article info
Publication history
Published online: May 27, 2016
Accepted:
May 18,
2016
Received in revised form:
May 16,
2016
Received:
September 14,
2015
Identification
Copyright
© Society of Biological Psychiatry, 2016.
ScienceDirect
Access this article on ScienceDirectLinked Article
- Scanning for Justice With Functional Magnetic Resonance ImagingBiological PsychiatryVol. 82Issue 4
- PreviewIf asked to predict the weight of a Major League baseball, you’d probably be able to do it rather easily; by weighing a representative sample, you could use the mean of your observations to predict the weight of the next ball to within 5 grams. By regulation, all balls must weigh between 142 and 149 grams—which is to say that if you guessed 145 grams, you would be right 100% of the time.
- Full-Text
- Preview
