Hyporesponsive Reward Anticipation in the Basal Ganglia following Severe Institutional Deprivation Early in Life

Journal of Cognitive Neuroscience - Tập 22 Số 10 - Trang 2316-2325 - 2010
Mitul A. Mehta1, Emma Gore-Langton1, Nicole I. Golembo1, Emma Colvert1, Steven Williams1, Edmund Sonuga‐Barke1,2,3
11King's College London, UK
22University of Southampton, UK
33University of Ghent, Belgium

Tóm tắt

AbstractSevere deprivation in the first few years of life is associated with multiple difficulties in cognition and behavior. However, the brain basis for these difficulties is poorly understood. Structural and functional neuroimaging studies have implicated limbic system structures as dysfunctional, and one functional imaging study in a heterogeneous group of maltreated individuals has confirmed the presence of abnormalities in the basal ganglia. Based on these studies and known dopaminergic abnormalities from studies in experimental animals using social isolation, we used a task of monetary reward anticipation to examine the functional integrity of brain regions previously shown to be implicated in reward processing. Our sample included a group of adolescents (n = 12) who had experienced global deprivation early in their lives in Romania prior to adoption into UK families. In contrast to a nonadopted comparison group (n = 11), the adoptees did not recruit the striatum during reward anticipation despite comparable performance accuracy and latency. These results show, for the first time, an association between early institutional deprivation and brain reward systems in humans and highlight potential neural vulnerabilities resulting from such exposures.

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Tài liệu tham khảo

Abler, 2007, Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fMRI study., Psychopharmacology (Berlin), 191, 823, 10.1007/s00213-006-0690-y

Ahmed, 1995, Social deprivation enhances the vulnerability of male Wistar rats to stressor- and amphetamine-induced behavioral sensitization., Psychopharmacology (Berlin), 117, 116, 10.1007/BF02245106

Alexander, 1986, Parallel organization of functionally segregated circuits linking the basal ganglia and cortex., Annual Review of Neuroscience, 9, 357, 10.1146/annurev.ne.09.030186.002041

Bjork, 2004, Incentive-elicited brain activation in adolescents: Similarities and differences from young adults., Journal of Neuroscience, 24, 1793, 10.1523/JNEUROSCI.4862-03.2004

Brett, 2002, Region of interest analysis using an SPM toolbox., Neuroimage, 16

Busche, 2004, Developmentally induced imbalance of dopaminergic fibre densities in limbic brain regions of gerbils (Meriones unguiculatus)., Journal of Neural Transmission, 111, 451, 10.1007/s00702-004-0106-2

Callicott, 2003, Complexity of prefrontal cortical dysfunction in schizophrenia: More than up or down., American Journal of Psychiatry, 160, 2209, 10.1176/appi.ajp.160.12.2209

Castle, 1999, Effects of qualities of early institutional care on cognitive attainment. E.R.A. Study Team. English and Romanian Adoptees., American Journal of Orthopsychiatry, 69, 424, 10.1037/h0080391

Cohen, 2009, Connectivity-based segregation of the human striatum predicts personality characteristics., Nature Neuroscience, 12, 32, 10.1038/nn.2228

Cooper, 2008, Valence and salience contribute to nucleus accumbens activation., Neuroimage, 39, 538, 10.1016/j.neuroimage.2007.08.009

D'Ardenne, 2008, BOLD responses reflecting dopaminergic signals in the human ventral tegmental area., Science, 319, 1264, 10.1126/science.1150605

Del Arco, 2004, Hyperactivity to novelty induced by social isolation is not correlated with changes in D2 receptor function and binding in striatum., Psychopharmacology (Berlin), 171, 148, 10.1007/s00213-003-1578-8

Dillon, 2009, Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood., Biological Psychiatry, 66, 206, 10.1016/j.biopsych.2009.02.019

Dreher, 2009, Variation in dopamine genes influences responsivity of the human reward system., Proceedings of the National Academy of Sciences, U.S.A., 106, 617, 10.1073/pnas.0805517106

Eluvathingal, 2006, Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study., Pediatrics, 117, 2093, 10.1542/peds.2005-1727

Ernst, 2009, A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes., Neuroscience and Biobehavioral Reviews, 33, 367, 10.1016/j.neubiorev.2008.10.009

Friston, 1995, Statistical parametric maps in functional imaging: A general linear approach., Human Brain Mapping, 2, 189, 10.1002/hbm.460020402

Fulford, 1998, Conditioned release of 5-hydroxytryptamine in vivo in the nucleus accumbens following isolation-rearing in the rat., Neuroscience, 83, 481, 10.1016/S0306-4522(97)00423-5

Fulford, 1998, Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat., Journal of Neurochemistry, 70, 384, 10.1046/j.1471-4159.1998.70010384.x

Gold, 2003, Linking reward expectation to behavior in the basal ganglia., Trends in Neurosciences, 26, 12, 10.1016/S0166-2236(02)00002-4

Goodman, 1997, The strengths and difficulties questionnaire: A research note., Journal of Child Psychology and Psychiatry and Allied Disciplines, 38, 581, 10.1111/j.1469-7610.1997.tb01545.x

Guyer, 2006, Behavioral alterations in reward system function: The role of childhood maltreatment and psychopathology., Journal of the American Academy of Child and Adolescent Psychiatry, 45, 1059, 10.1097/01.chi.0000227882.50404.11

Haber, 2000, Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum., Journal of Neuroscience, 20, 2369, 10.1523/JNEUROSCI.20-06-02369.2000

Haber, 1999, The concept of the ventral striatum in nonhuman primates., Annals of the New York Academy of Sciences, 877, 33, 10.1111/j.1749-6632.1999.tb09259.x

Hall, 1998, Isolation rearing in rats: Pre- and postsynaptic changes in striatal dopaminergic systems., Pharmacology, Biochemistry and Behavior, 59, 859, 10.1016/S0091-3057(97)00510-8

Hampton, 2007, Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex., Neuron, 55, 545, 10.1016/j.neuron.2007.07.022

Howes, 2000, Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: Relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala–striatal FOS expression., Psychopharmacology (Berlin), 151, 55, 10.1007/s002130000451

Jones, 1992, Dopaminergic and serotonergic function following isolation rearing in rats: Study of behavioural responses and postmortem and in vivo neurochemistry., Pharmacology, Biochemistry and Behavior, 43, 17, 10.1016/0091-3057(92)90635-S

Jones, 1990, Increased sensitivity to amphetamine and reward-related stimuli following social isolation in rats: Possible disruption of dopamine-dependent mechanisms of the nucleus accumbens., Psychopharmacology, 102, 364, 10.1007/BF02244105

Juckel, 2006, Dysfunction of ventral striatal reward prediction in schizophrenia., Neuroimage, 29, 409, 10.1016/j.neuroimage.2005.07.051

Kalivas, 2005, The neural basis of addiction: A pathology of motivation and choice., American Journal of Psychiatry, 162, 1403, 10.1176/appi.ajp.162.8.1403

Knutson, 2001, Anticipation of increasing monetary reward selectively recruits nucleus accumbens., Journal of Neuroscience, 21, RC159, 10.1523/JNEUROSCI.21-16-j0002.2001

Knutson, 2004, Amphetamine modulates human incentive processing., Neuron, 43, 261, 10.1016/j.neuron.2004.06.030

Knutson, 2007, Linking nucleus accumbens dopamine and blood oxygenation., Psychopharmacology (Berlin), 191, 813, 10.1007/s00213-006-0686-7

Kobayashi, 2002, Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex., Journal of Neurophysiology, 87, 1488, 10.1152/jn.00472.2001

Lauwereyns, 2002, A neural correlate of response bias in monkey caudate nucleus., Nature, 418, 413, 10.1038/nature00892

Martin-Soelch, 2009, Is depression associated with dysfunction of the central reward system?, Biochemical Society Transactions, 37, 313, 10.1042/BST0370313

Martinez, 2003, Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: Amphetamine-induced dopamine release in the functional subdivisions of the striatum., Journal of Cerebral Blood Flow and Metabolism, 23, 285, 10.1097/01.WCB.0000048520.34839.1A

Mehta, 2009, Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian Adoptees Study Pilot., Journal of Child Psychology and Psychiatry, 50, 943, 10.1111/j.1469-7610.2009.02084.x

Morris, 2006, Midbrain dopamine neurons encode decisions for future action., Nature Neuroscience, 9, 1057, 10.1038/nn1743

Nelson, 2009, Adverse rearing experiences enhance responding to both aversive and rewarding stimuli in juvenile rhesus monkeys., Biological Psychiatry, 66, 702, 10.1016/j.biopsych.2009.04.007

Nestler, 2006, The mesolimbic dopamine reward circuit in depression., Biological Psychiatry, 59, 1151, 10.1016/j.biopsych.2005.09.018

O'Doherty, 2004, Reward representations and reward-related learning in the human brain: Insights from neuroimaging., Current Opinion in Neurobiology, 14, 769, 10.1016/j.conb.2004.10.016

Peters, 2005, Social isolation rearing affects prefrontal cortical response to ventral tegmental area stimulation., Biological Psychiatry, 57, 1205, 10.1016/j.biopsych.2005.02.011

Phillips, 1994, Isolation rearing impairs the reinforcing efficacy of intravenous cocaine or intra-accumbens d-amphetamine: Impaired response to intra-accumbens D1 and D2/D3 dopamine receptor antagonists., Psychopharmacology (Berlin), 115, 419, 10.1007/BF02245085

Phillips, 1995, Analysis of the effects of intra-accumbens SKF-38393 and LY-171555 upon the behavioural satiety sequence., Psychopharmacology (Berlin), 117, 82, 10.1007/BF02245102

Phillips, 1994, Isolation rearing enhances the locomotor response to cocaine and a novel environment, but impairs the intravenous self-administration of cocaine., Psychopharmacology (Berlin), 115, 407, 10.1007/BF02245084

Powell, 2003, Dopamine depletion of the nucleus accumbens reverses isolation-induced deficits in prepulse inhibition in rats., Neuroscience, 119, 233, 10.1016/S0306-4522(03)00122-2

Pryce, 2004, Evidence for altered monoamine activity and emotional and cognitive disturbance in marmoset monkeys exposed to early life stress., Annals of the New York Academy of Sciences, 1032, 245, 10.1196/annals.1314.030

Roesch, 2007, Neuronal activity related to anticipated reward in frontal cortex: Does it represent value or reflect motivation?, Annals of the New York Academy of Sciences, 1121, 431, 10.1196/annals.1401.004

Rubia, 2005, Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD., American Journal of Psychiatry, 162, 1067, 10.1176/appi.ajp.162.6.1067

Rutter, 1998, Developmental catch-up, and deficit, following adoption after severe global early privation. English and Romanian Adoptees (ERA) Study Team., Journal of Child Psychology and Psychiatry, 39, 465, 10.1017/S0021963098002236

Rutter, 2009, Effects of profound early institutional deprivation: An overview of findings from a UK longitudinal study of Romanian adoptees., International advances in adoption research for practice, 147, 10.1002/9780470741276.ch7

Rutter, 2007, Early adolescent outcomes for institutionally-deprived and non-deprived adoptees: I. Disinhibited attachment., Journal of Child Psychology and Psychiatry, 48, 17, 10.1111/j.1469-7610.2006.01688.x

Rutter, 2007, Early adolescent outcomes of institutionally deprived and non-deprived adoptees: III. Quasi-autism., Journal of Child Psychology and Psychiatry, 48, 1200, 10.1111/j.1469-7610.2007.01792.x

Rutter, 2001, Specificity and heterogeneity in children's responses to profound institutional privation., British Journal of Psychiatry, 179, 97, 10.1192/bjp.179.2.97

Sahakian, 1975, The effects of psychomotor stimulants on stereotypy and locomotor activity in socially-deprived and control rats., Brain Research, 84, 195, 10.1016/0006-8993(75)90975-0

Salamone, 2002, Motivational views of reinforcement: Implications for understanding the behavioral functions of nucleus accumbens dopamine., Behavioural Brain Research, 137, 3, 10.1016/S0166-4328(02)00282-6

Salamone, 2007, Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits., Psychopharmacology (Berlin), 191, 461, 10.1007/s00213-006-0668-9

Scheres, 2007, Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder., Biological Psychiatry, 61, 720, 10.1016/j.biopsych.2006.04.042

Schott, 2008, Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release., Journal of Neuroscience, 28, 14311, 10.1523/JNEUROSCI.2058-08.2008

Schultz, 2003, The role of the fusiform face area in social cognition: Implications for the pathobiology of autism., Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 358, 415, 10.1098/rstb.2002.1208

Schultz, 2006, Behavioral theories and the neurophysiology of reward., Annual Review of Psychology, 57, 87, 10.1146/annurev.psych.56.091103.070229

Sonuga-Barke, 2008, Is sub-nutrition necessary for a poor outcome following early institutional deprivation?, Developmental Medicine and Child Neurology, 50, 664, 10.1111/j.1469-8749.2008.03065.x

Stevens, 2006, A consideration of the potential role of genetic factors in individual differences in response to early institutional deprivation: The case of inattention/overactivity in the English and Romanian adoptees study., The Association for Child and Adolescent Mental Health, Occasional Papers. Genetics: Impact on Current Child and Adolescent Mental Health, 25, 66

Strohle, 2008, Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder., Neuroimage, 39, 966, 10.1016/j.neuroimage.2007.09.044

Tzourio-Mazoyer, 2002, Automated anatomical labelling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single subject brain., Neuroimage, 15, 273, 10.1006/nimg.2001.0978

Voorn, 2004, Putting a spin on the dorsal–ventral divide of the striatum., Trends in Neurosciences, 27, 468, 10.1016/j.tins.2004.06.006

Weiss, 2001, Early social isolation, but not maternal separation, affects behavioral sensitization to amphetamine in male and female adult rats., Pharmacology, Biochemistry and Behavior, 70, 397, 10.1016/S0091-3057(01)00626-8

Wise, 2004, Dopamine, learning and motivation., Nature Reviews Neuroscience, 5, 483, 10.1038/nrn1406

Wise, 1982, Action of drugs of abuse on brain reward systems: An update with specific attention to opiates., Pharmacology, Biochemistry and Behavior, 17, 239, 10.1016/0091-3057(82)90076-4

Wrase, 2007, Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics., Neuroimage, 35, 787, 10.1016/j.neuroimage.2006.11.043