Patients with major depressive disorder exhibit reduced reward size coding in the striatum

Takamura, Masahiro; Okamoto, Yasumasa; Okada, Go; Toki, Shigeru; Yamamoto, Tetsuya; Ichikawa, Naho; Mori, Asako; Minagawa, Hideaki; Takaishi, Yoshiyuki; Fujii, Yasumasa; Kaichi, Yoko; Akiyama, Yuji; Awai, Kazuo; Yamawaki, Shigeto

doi:10.1016/j.pnpbp.2017.07.006

Cited by 66 publications

(34 citation statements)

References 28 publications

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“…FMRI activation of the NAcc was lower in the MDD group than in the CTL group, consistent with previous studies (Pizzagalli et al, 2009;Takamura et al, 2017;Ubl et al, 2015a). The striatum, especially the NAcc, is a core node of the reward system, and its activity is related to reward information from external stimuli and individual goal-oriented behavior (Kohls et al, 2012).…”

Section: Discussionsupporting

confidence: 89%

“…Dysfunction of the dopaminergic system has been linked with the pathophysiology of Major Depressive Disorder (MDD). Several researchers have reported reductions in fMRI activation in the striatum in MDD patients during reward anticipation (Pizzagalli et al, 2009;Takamura et al, 2017;Ubl et al, 2015b;Whitton et al, 2015), while other investigators have reported no MDD-associated differences in the striatum (Knutson et al, 2008). PET studies have implicated aberrant baseline dopamine binding potential in the striatum in MDD (Hamilton et al, 2018;Hirvonen et al, 2008a;Meyer et al, 2006;Montgomery et al, 2007a;Sun and Sun, 2017;Yatham et al, 2002), and their findings are similarly inconsistent, with reports of both increased and decreased dopamine binding.…”

Section: Introductionmentioning

confidence: 99%

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Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI

Zhang

Wang

Hamilton

et al. 2019

Preprint

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The interaction of the midbrain dopaminergic system and the striatum is implicated in reward processing; it is still unknown, however, how this interaction is altered in Major Depressive Disorder (MDD). In the current study, we related the dopamine release/binding inferred by [ 11 C] Raclopride functional Positron Emission Tomography (fPET) to neural activity monitored by blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) in adults diagnosed with MDD and healthy controls (CTL). Participants completed a monetary incentive delay (MID) task during simultaneous [ 11 C] Raclopride fPET and fMRI. Instead of the usual kinetic modeling method for analyzing dynamic PET time activity curves (TACs), we used a simpler general linear model (GLM) approach, which includes introducing a fPET dopamine activation response function to model changes in the TAC associated with the MID task. In addition, using simulations, we show that the GLM approach has several advantages over kinetic modeling. This is achieved without invoking erroneous steady-state assumptions or selecting a suitable reference region. Our results include the observation of both decreased fMRI activation and dopamine release/binding in the striatum in the MDD cohort, implying a reduced reward processing capacity in MDD. Furthermore, in the MDD group, individuals with lower fMRI activations in the right middle putamen and ventral medial prefrontal cortex (vmPFC) had higher reflection rumination scores, and individuals with lower dopamine release/binding in the left putamen and the right nucleus accumbens (NAcc) also had higher reflection rumination scores.Significant cross-modal inter-subject and intra-subject correlations of dopamine release/binding 3 and fMRI activation were observed in the CTL group, but not in the MDD group. The intrasubject correlation of the two modalities was negatively associated with reflection rumination scores in the CTL group, indicating that decoupling of the dopaminergic system and striatum may be important in the pathophysiology of MDD.

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Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI

Zhang

Wang

Hamilton

et al. 2019

Preprint

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“…Using the MID to assess neural responses during anticipation of rewards following cue presentation, three fMRI studies observed VS hypoactivation during reward anticipation in MDD (Arrondo et al, 2015 ; Hagele et al, 2015 ; Takamura et al, 2017 ). Additionally, VS hypoactivation during reward anticipation has been shown to be associated with both current and future subthreshold and clinical MDD (Stringaris et al, 2015 ) and was observed in a sample of unmedicated MDD participants (Ubl, Kuehner, Kirsch, Ruttorf, Diener, et al, 2015b ).…”

Section: Resultsmentioning

confidence: 99%

“…The MID involves components of various reward processes, but striatal dopamine activity is associated with reward coding during anticipation (Abler, Walter, Erk, Kammerer, Spitzer, 2006). Other studies using the MID in MDD participants have also found patterns of striatal hypoactivation during reward anticipation, in both the NAc (Misaki, Suzuki, Savitz, Drevets, & Bodurka, 2016) and the putamen (Pizzagalli et al, 2009;Takamura et al, 2017), with one study using an unmedicated MDD sample (Pizzagalli et al, 2009). In agreement with studies using the MID, studies using the card guessing task have reported VS hypoactivation during reward anticipation in children with MDD (Olino et al, 2011) and lower striatal reactivity to rewards in adolescents (Insel, Glenn, Nock, & Somerville, 2018).…”

Section: Reward Anticipationmentioning

confidence: 99%

Characterizing anhedonia: A systematic review of neuroimaging across the subtypes of reward processing deficits in depression

Borsini

Wallis

Zunszain

et al. 2020

Cogn Affect Behav Neurosci

111

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Anhedonia is a key symptom of major depressive disorder (MDD) and comprises behavioural deficits in three reward processing subtypes: reward liking, reward wanting, and reward learning. However, neuroimaging findings regarding the neural abnormalities underpinning these deficits are complex. We have conducted a systematic review to update, reframe and summarize neuroimaging findings across the three subtypes of anhedonia in MDD. Using PubMed, The Cochrane Library, PsycINFO, and Web of Science databases, we identified 59 fMRI studies comparing participants with current or remitted MDD with controls, using reward processing tasks. For reward liking and wanting, striatal hypoactivation was observed, alongside hypoactivation and hyperactivation across frontal regions. For reward learning, blunted frontostriatal sensitivity to positive feedback was observed. These findings highlight the importance of studying anhedonia not only as a clinical manifestation but also as a neurobiological mechanism underlying depressive disorder and other broader psychiatric conditions. Keywords Anhedonia. Depression. Neuroimaging. fMRI. Reward processing Major depressive disorder (MDD) is both common, with a lifetime prevalence of 16.6% in the USA (Kessler, Petukhova, Sampson, Zaslavsky, & Wittchen, 2012), and consequential, being the second leading contributor to global years lived with disability (YLDs) worldwide (Ferrari et al., 2013). Anhedonia is one of two key symptoms required for a diagnosis of MDD in the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5; American Psychiatric Association, 2013), and is defined as 'markedly diminished interest or pleasure in all, or almost all, activities most of the day, nearly every day' (American Psychiatric Association, 2013), and so represents a deficit in reward processing. In a study examining the factor structure for DSM-IV, MDD symptoms in a sample 2,615 army recruits, the best fit for the data indicated that MDD consisted of both a somatic and nonsomatic component (Elhai et al., 2012), and anhedonia had the second highest factor weighting (Beta = 0.76) for the nonsomatic component (after depressed mood), as well as the second highest factor weighting of all symptoms (Elhai et al., 2012). This suggests that anhedonia is a core feature of depression. Anhedonia is a symptom which warrants attention; indeed, reward processing deficits are associated with increased risk of new onset MDD (Rawal, Collishaw, Thapar, & Rice, 2013), anhedonia may precede illness onset, and, moreover, it can often persist past the remission of other depressive symptoms (Schrader, 1997), as do deficits on reward processing tasks (Pechtel, Dutra, Goetz, & Pizzagalli, 2013). Three subtypes of anhedonia In DSM-5, anhedonia comprises deficits in hedonic experience of rewards and motivation for rewards (American Psychiatric Association, 2013). However, reviews have called for research to conceptualize anhedonia as comprising deficits across three partially separable subtypes of reward processing:

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“…Both components of motivation, when expressed in excess or insufficiency, can be associated with maladaptive behavior. Indeed, several studies have shown that individuals with major depressive disorder and schizophrenia both lack motivation for rewards ( Takamura et al, 2017 ; Whitton, Treadway & Pizzagalli, 2015 ), whereas individuals with substance use disorders have uncontrolled motivation for substance seeking but decreased motivation for alternative natural rewards ( Baker et al, 2017 ). There is also evidence individuals with anxiety disorders are characterized by harm avoidance ( Ottenbreit, Dobson & Quigley, 2014 ; Wright, Lebell & Carleton, 2016 ), whereas individuals with antisocial behavior tend to be insensitive to punishment ( Byrd, Loeber & Pardini, 2014 ; Loney et al, 2003 ).…”

Section: Introductionmentioning

confidence: 99%

Loss anticipation and outcome during theMonetary Incentive Delay Task: a neuroimaging systematic review and meta-analysis

Dugré

Dumais

Bitar

et al. 2018

PeerJ

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BackgroundReward seeking and avoidance of punishment are key motivational processes. Brain-imaging studies often use the Monetary Incentive Delay Task (MIDT) to evaluate motivational processes involved in maladaptive behavior. Although the bulk of research has been done on the MIDT reward events, little is known about the neural basis of avoidance of punishment. Therefore, we conducted a meta-analysis of brain activations during anticipation and receipt of monetary losses in healthy controls.MethodsAll functional neuro-imaging studies using the MIDT in healthy controls were retrieved using PubMed, Google Scholar & EMBASE databases. Functional neuro-imaging data was analyzed using the Seed-based d Mapping Software.ResultsThirty-five studies met the inclusion criteria, comprising 699 healthy adults. In both anticipation and loss outcome phases, participants showed large and robust activations in the bilateral striatum, (anterior) insula, and anterior cingulate gyrus relatively to Loss > Neutral contrast. Although relatively similar activation patterns were observed during the two event types, they differed in the pattern of prefrontal activations: ventro-lateral prefrontal activations were observed during loss anticipation, while medial prefrontal activations were observed during loss receipt.DiscussionConsidering that previous meta-analyses highlighted activations in the medial prefrontal cortex/anterior cingulate cortex, the anterior insula and the ventral striatum, the current meta-analysis highlighted the potential specificity of the ventro-lateral prefrontal regions, the median cingulate cortex and the amygdala in the loss events. Future studies can rely on these latter results to examine the neural correlates of loss processing in psychiatric populations characterized by harm avoidance or insensitivity to punishment.

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Patients with major depressive disorder exhibit reduced reward size coding in the striatum

Abstract: Patients with MDD exhibit reduced ability to modulate neural response when adjusting for variable amount of reward. This result suggests that reward size coding in the striatum may represent a neural correlate of motivational anhedonia in MDD patients.

Cited by 66 publications

References 28 publications

Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI

Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI

Characterizing anhedonia: A systematic review of neuroimaging across the subtypes of reward processing deficits in depression

Loss anticipation and outcome during theMonetary Incentive Delay Task: a neuroimaging systematic review and meta-analysis

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