Amphetamine Sensitization Alters Reward Processing in the Human Striatum and Amygdala
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{"title"=>"Amphetamine sensitization alters reward processing in the human striatum and amygdala", "type"=>"journal", "authors"=>[{"first_name"=>"Owen G.", "last_name"=>"O'Daly", "scopus_author_id"=>"8652547800"}, {"first_name"=>"Daniel", "last_name"=>"Joyce", "scopus_author_id"=>"8840173400"}, {"first_name"=>"Derek K.", "last_name"=>"Tracy", "scopus_author_id"=>"13604870100"}, {"first_name"=>"Adnan", "last_name"=>"Azim", "scopus_author_id"=>"36514137400"}, {"first_name"=>"Klaas E.", "last_name"=>"Stephan", "scopus_author_id"=>"7102375486"}, {"first_name"=>"Robin M.", "last_name"=>"Murray", "scopus_author_id"=>"35406239400"}, {"first_name"=>"Sukhwinder S.", "last_name"=>"Shergill", "scopus_author_id"=>"35433190700"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84899541896", "sgr"=>"84899541896", "pui"=>"372971475", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"24717936", "doi"=>"10.1371/journal.pone.0093955"}, "id"=>"5edae097-89e8-3b60-b22a-cb84cdd66d64", "abstract"=>"Dysregulation of mesolimbic dopamine transmission is implicated in a number of psychiatric illnesses characterised by disruption of reward processing and goal-directed behaviour, including schizophrenia, drug addiction and impulse control disorders associated with chronic use of dopamine agonists. Amphetamine sensitization (AS) has been proposed to model the development of this aberrant dopamine signalling and the subsequent dysregulation of incentive motivational processes. However, in humans the effects of AS on the dopamine-sensitive neural circuitry associated with reward processing remains unclear. Here we describe the effects of acute amphetamine administration, following a sensitising dosage regime, on blood oxygen level dependent (BOLD) signal in dopaminoceptive brain regions during a rewarded gambling task performed by healthy volunteers. Using a randomised, double-blind, parallel-groups design, we found clear evidence for sensitization to the subjective effects of the drug, while rewarded reaction times were unchanged. Repeated amphetamine exposure was associated with reduced dorsal striatal BOLD signal during decision making, but enhanced ventromedial caudate activity during reward anticipation. The amygdala BOLD response to reward outcomes was blunted following repeated amphetamine exposure. Positive correlations between subjective sensitization and changes in anticipation- and outcome-related BOLD signal were seen for the caudate nucleus and amygdala, respectively. These data show for the first time in humans that AS changes the functional impact of acute stimulant exposure on the processing of reward-related information within dopaminoceptive regions. Our findings accord with pathophysiological models which implicate aberrant dopaminergic modulation of striatal and amygdala activity in psychosis and drug-related compulsive disorders.", "link"=>"http://www.mendeley.com/research/amphetamine-sensitization-alters-reward-processing-human-striatum-amygdala", "reader_count"=>77, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>14, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>5, "Student > Master"=>14, "Other"=>6, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>14, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>5, "Student > Master"=>14, "Other"=>6, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>1, "Agricultural and Biological Sciences"=>8, "Medicine and Dentistry"=>12, "Neuroscience"=>18, "Sports and Recreations"=>1, "Business, Management and Accounting"=>1, "Psychology"=>25, "Social Sciences"=>5, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>12}, "Neuroscience"=>{"Neuroscience"=>18}, "Social Sciences"=>{"Social Sciences"=>5}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Psychology"=>{"Psychology"=>25}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Computer Science"=>{"Computer Science"=>2}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Japan"=>1, "United Kingdom"=>1, "Mexico"=>1, "Switzerland"=>1, "Germany"=>1, "Spain"=>2}, "group_count"=>9}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1457396"], "description"=>"<div><p>Dysregulation of mesolimbic dopamine transmission is implicated in a number of psychiatric illnesses characterised by disruption of reward processing and goal-directed behaviour, including schizophrenia, drug addiction and impulse control disorders associated with chronic use of dopamine agonists. Amphetamine sensitization (AS) has been proposed to model the development of this aberrant dopamine signalling and the subsequent dysregulation of incentive motivational processes. However, in humans the effects of AS on the dopamine-sensitive neural circuitry associated with reward processing remains unclear. Here we describe the effects of acute amphetamine administration, following a sensitising dosage regime, on blood oxygen level dependent (BOLD) signal in dopaminoceptive brain regions during a rewarded gambling task performed by healthy volunteers. Using a randomised, double-blind, parallel-groups design, we found clear evidence for sensitization to the subjective effects of the drug, while rewarded reaction times were unchanged. Repeated amphetamine exposure was associated with reduced dorsal striatal BOLD signal during decision making, but enhanced ventromedial caudate activity during reward anticipation. The amygdala BOLD response to reward outcomes was blunted following repeated amphetamine exposure. Positive correlations between subjective sensitization and changes in anticipation- and outcome-related BOLD signal were seen for the caudate nucleus and amygdala, respectively. These data show for the first time in humans that AS changes the functional impact of acute stimulant exposure on the processing of reward-related information within dopaminoceptive regions. Our findings accord with pathophysiological models which implicate aberrant dopaminergic modulation of striatal and amygdala activity in psychosis and drug-related compulsive disorders.</p></div>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "sensitization", "alters", "striatum"], "article_id"=>993301, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amphetamine_Sensitization_Alters_Reward_Processing_in_the_Human_Striatum_and_Amygdala_/993301", "title"=>"Amphetamine Sensitization Alters Reward Processing in the Human Striatum and Amygdala", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-04-09 03:29:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1457376"], "description"=>"<p>(Top) The task had a blocked design where gambling blocks were interleaved with control blocks. Each block consisted of 5 trials, each of 12 seconds length. (Middle) Each trial was 12 seconds long and included a 2 second decision period where a wheel (see bottom) was presented which indicated the perceived probability of winning on this trial. During gambling trials participants were required to make a choice (Red or Black) or they would simply lose the compulsory £1 wager automatically. In the control condition, subject were still asked to make a choice but were limited to colours other than Red and Black and no money was wagered. Following the decision, a variable anticipatory delay (4–7 seconds) preceded a 3–6 second outcome phase where the participant was informed of the outcome of the trial and their balance was amended. Three wheel types were available, each indicating the probability of winning the participant should expect on that trial.</p>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "rewarded", "gambling"], "article_id"=>993283, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955.g001", "stats"=>{"downloads"=>4, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_Design_of_the_Rewarded_Gambling_Task_/993283", "title"=>"Experimental Design of the Rewarded Gambling Task.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-09 03:29:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1457395"], "description"=>"<p>To illustrate the nature of the interaction effect, the middle panel shows parameter estimates (in the order placebo at scan 1, placebo at scan 2, AS at scan 1 (before sensitisation)), AS at scan 2 (after sensitisation) from peak voxel within the right amygdala. Additionally, the graph on the right shows the correlation between sensitisation-related change in amygdala BOLD signal during outcome-processing and the change in subjective report of amphetamine-like experience. All parameter estimates reflect the mean response in arbitrary BOLD units. Results are shown with the standard error of the mean.</p>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "amygdala", "gambling"], "article_id"=>993300, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955.g005", "stats"=>{"downloads"=>3, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significant_Group_215_Session_interaction_p_lt_0_05_corrected_in_the_right_amygdala_during_the_outcome_phase_i_e_Wins_gt_Loss_of_our_gambling_task_left_panel_/993300", "title"=>"Significant Group × Session interaction (p<0.05, corrected) in the right amygdala during the outcome phase (i.e. Wins>Loss) of our gambling task (left panel).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-09 03:29:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1457388"], "description"=>"<p>The right panel shows parameter estimates (in the order placebo at scan 1, placebo at scan 2, AS at scan 1 (before sensitisation), AS at scan 2 (after sensitisation)) from the mean from an associative striatal ROI. Note that this plot is merely used to illustrate the nature of the interaction effect. All parameter estimates reflect the mean response in arbitrary BOLD units. Results are shown with the standard error of the mean.</p>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "caudate", "nucleus", "decision-making", "gambling"], "article_id"=>993294, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955.g003", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significant_Group_215_Session_interaction_in_the_caudate_nucleus_during_the_decision_making_phase_of_our_gambling_task_p_lt_0_05_corrected_/993294", "title"=>"Significant Group × Session interaction in the caudate nucleus during the decision-making phase of our gambling task (p<0.05, corrected).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-09 03:29:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1457385"], "description"=>"<p>Parameter estimates for key dopaminergic and reward-related areas showing a significant main effect of task (right panel). Lower Panel: Brain regions where BOLD signal was modulated by reward probability the placebo group (left panel). Parameter estimates from the occipital cortex and precuneus, regions that display a significant main effect of reward probability. All parameter estimates reflect the mean response in arbitrary BOLD units. Results are shown with the standard error of the mean.</p>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "regions", "displaying", "phases", "wins", "placebo"], "article_id"=>993291, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Upper_Panel_Brain_regions_identified_as_displaying_sensitivity_to_the_task_phases_i_e_decision_anticipation_wins_and_losses_in_the_placebo_group_left_panel_/993291", "title"=>"Upper Panel: Brain regions identified as displaying sensitivity to the task phases (i.e. decision, anticipation, wins and losses) in the placebo group (left panel).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-09 03:29:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1457392"], "description"=>"<p>To illustrate the nature of the interaction effect, the middle panel shows parameter estimates (in the order placebo at scan 1, placebo at scan 2, AS at scan 1 (before sensitisation), AS at scan 2 (after sensitisation) from the mean response within an associative striatal ROI. The graph on the right shows the correlation between sensitisation-related change in striatal BOLD signal during anticipation and the change in subjective response to amphetamine. All parameter estimates reflect the mean response in arbitrary BOLD units. Results are shown with the standard error of the mean.</p>", "links"=>[], "tags"=>["neuroscience", "cognitive science", "cognition", "memory", "Cognitive psychology", "attention", "learning", "reasoning", "Behavioral neuroscience", "Cognitive neuroscience", "Learning and memory", "neuroimaging", "neuropsychology", "psychology", "behavior", "habits", "Human performance", "neural networks", "Mental health and psychiatry", "Substance-related disorders", "Substance abuse", "psychoses", "schizophrenia", "neurology", "Neurobiology of disease and regeneration", "anticipation", "gambling"], "article_id"=>993298, "categories"=>["Biological Sciences"], "users"=>["Owen G. O’Daly", "Daniel Joyce", "Derek K. Tracy", "Adnan Azim", "Klaas E. Stephan", "Robin M. Murray", "Sukhwinder S. Shergill"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093955.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significant_Group_215_Session_interaction_p_lt_0_05_corrected_during_the_anticipation_phase_of_our_gambling_task_left_panel_/993298", "title"=>"Significant Group × Session interaction (p<0.05, corrected) during the anticipation phase of our gambling task (left panel).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-09 03:29:33"}

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