Elsevier

Biological Psychology

Volume 123, February 2017, Pages 62-73
Biological Psychology

Ventral Striatum Functional Connectivity during Rewards and Losses and Symptomatology in Depressed Patients

https://doi.org/10.1016/j.biopsycho.2016.11.004Get rights and content

Highlights

  • We examined the striatal network, which encodes natural rewards, in depressed and healthy adults.

  • Depressed adults show high striatal connectivity with neocortical areas during losses versus rewards.

  • Suicidality, anhedonia, and depressive mood are associated with higher VS connectivity to the Prefrontal Cortex.

Abstract

Background

The ventral striatum (VS) and striatal network supports goal motivated behavior. Identifying how depressed patients differ in their striatal network during the processing of emotionally salient events is a step towards uncovering biomarkers for diagnosis and treatment.

Methods

38 depressed and 30 healthy adults completed a task that examined brain activation to the anticipation and receipt of monetary rewards and losses. Data were collected using a 3T Siemens Trio scanner. Functional connectivity differences were examined with seeds in the Left or Right VS. FC estimates were regressed on specific symptoms.

Results

Depressed patients displayed higher functional connectivity between the VS and midline cortical areas during loss versus reward trials. Anhedonia and depressed mood were associated to fairly similar striatal circuits but suicidality was associated to a unique VS-midline structures coupling, while depression severity was linked to higher VS to caudate and precuneus connectivity during loss versus reward trials.

Conclusions

Depression is characterized by excessive VS coupling to cognitive control and associative networks during losses versus rewards. High VS to midline cortical structures coupling may index suicidality.

Section snippets

Background

Preferential processing of negative versus positive events, such as monetary losses and rewards, is a hallmark of depressive states. Theories of depression have posited that vulnerable and depressed individuals exhibit a cognitive triad comprised by rigid negative attributions regarding the self, one’s environment, and one’s future (Beck, 1972; Beck, Brown, Steer, Eidelson, & Riskind, 1987), including persistent cognitive elaboration regarding flaws, failures and negative events, i.e.

Participants

Recruitment took place at the Western Psychiatric Institute and Clinic, Pittsburgh, and through advertisements. Subjects were evaluated with the Structured Clinical Interview for DSM-IV-Research-Version (SCID-P) (First, Spitzer, Gibbon, & Williams, 1995) and scanned in an MRI. Participants completed the Structured Clinical Interview for Mood Spectrum (SCI-MOODS) which yields continuous scale measures of mood symptoms such as depressed mood, anhedonia, and suicide thoughts (Rothwell & Stock, 1982

Corticostriatal functional connectivity in depressed versus healthy adults

Table 2 and Fig. 2 shows a main effect of group yielded by the 2 (group) by 6 (contrasts) GLM, which showed that compared to controls, depressed patients had large neural areas and significant peaks of BOLD signal coupled to the left and right VS during all negative versus all positive outcomes. These areas of increased coupling with the VS were primarily right midline cortical structures including the precuneus, and areas within the PFC (i.e., ACC and BA10). Increased VS to left caudate and

Discussion

This study compared the striatal network of depressed patients versus healthy control adults during the processing of positive and negative monetary outcomes. It also examined whether the strength of connectivity in the striatal network was associated with self-report ratings of anhedonia, depressed mood, suicidality and severity of depression.

Our first hypothesis, which predicted higher PFC-VS coupling for losses versus earnings among depressed participants, was confirmed. Our results (Fig. 2,

Financial disclosures

Dr. Mary Phillips is a representative for Roche Pharmaceuticals. No other author have biomedical finantial interests or potential conflicts of interest.

Acknowledgements

This research was supported by a NIMH, K01MH092601 to the first author and by an NMH, R01MH076971 to the last author. We are very grateful to Drs. Tom Zeffiro and Kathleen Thomas: key mentors and supporters of the first author’s K award application and progress. VAD acknowledges support from R01s, MH059299 and MH111177.

References (98)

  • K.J. Friston et al.

    Psychophysiological and modulatory interactions in neuroimaging

    Neuroimage

    (1997)
  • P.G. Gasquoine

    Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging

    Neuroscience and Biobehavioral Reviews

    (2013)
  • I.H. Gotlib et al.

    Biased information processing as a vulnerability factor for depression

    Behavior Therapy

    (1998)
  • J.A. Grahn et al.

    The cognitive functions of the caudate nucleus

    Progress in Neurobiology

    (2008)
  • A.M. Graybiel

    The basal ganglia: Learning new tricks and loving it

    Current Opinion in Neurobiology

    (2005)
  • J.P. Hamilton et al.

    Neural substrates of increased memory sensitivity for negative stimuli in major depression

    Biological Psychiatry

    (2008)
  • T.C. Ho et al.

    Functional connectivity of negative emotional processing in adolescent depression

    Journal of Affective Disorders

    (2014)
  • J.B. Hutchinson et al.

    Increased functional connectivity between dorsal posterior parietal and ventral occipitotemporal cortex during uncertain memory decisions

    Neurobiology of Learning and Memory

    (2015)
  • A.E. Kelley

    Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning

    Neuroscience and Biobehavioral Reviews

    (2004)
  • S.I. Kim

    Neuroscientific model of motivational process

    Frontiers in Psychology

    (2013)
  • J.E. LeDoux

    Emotional memory systems in the brain

    Behavioural Brain Research

    (1993)
  • S.N. Light et al.

    Reduced right ventrolateral prefrontal cortex activity while inhibiting positive affect is associated with improvement in hedonic capacity after 8 weeks of antidepressant treatment in major depressive disorder

    Biological Psychiatry

    (2011)
  • W.R. Marchand et al.

    Striatal and cortical midline circuits in major depression: Implications for suicide and symptom expression

    Progress in Neuro-Psychopharmacology & Biological Psychiatry

    (2012)
  • A. McGirr et al.

    An examination of DSM-IV depressive symptoms and risk for suicide completion in major depressive disorder: A psychological autopsy study

    Journal of Affective Disorders

    (2007)
  • L. Nrugham et al.

    Predictors of suicidal acts across adolescence: Influences of familial, peer and individual factors

    Journal of Affective Disorders

    (2008)
  • J.P. O’Doherty et al.

    Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum

    Neuron

    (2006)
  • J.P. O’Doherty

    Reward representations and reward-related learning in the human brain: Insights from neuroimaging

    Current Opinion in Neurobiology

    (2004)
  • K.L. Phan et al.

    Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI

    Neuroimage

    (2002)
  • N. Ramnani et al.

    Prediction error for free monetary reward in the human prefrontal cortex

    Neuroimage

    (2004)
  • N.J. Rothwell et al.

    Effects of early overnutrition and undernutrition in rats on the metabolic responses to overnutrition in later life

    Journal of Nutrition

    (1982)
  • C.E. Schiller et al.

    Remitted major depression is characterized by reduced prefrontal cortex reactivity to reward loss

    Journal of Affective Disorders

    (2013)
  • A. Shenhav et al.

    The expected value of control: An integrative theory of anterior cingulate cortex function

    Neuron

    (2013)
  • G.J. Siegle et al.

    Can't shake that feeling: Event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals

    Biological Psychiatry

    (2002)
  • J. Sturup et al.

    Violent behaviour by general psychiatric patients in Sweden – validation of Classification of Violence Risk (COVR) software

    Psychiatry Research

    (2011)
  • C.Y. Sylvester et al.

    Switching attention and resolving interference: FMRI measures of executive functions

    Neuropsychologia

    (2003)
  • E.M. Tricomi et al.

    Modulation of caudate activity by action contingency

    Neuron

    (2004)
  • E.S. Winer et al.

    Anhedonia predicts suicidal ideation in a large psychiatric inpatient sample

    Psychiatry Research

    (2014)
  • H. Zhang et al.

    Dysfunction of neural circuitry in depressive patients with suicidal behaviors: A review of structural and functional neuroimaging studies

    Progress in Neuro-Psychopharmacology and Biological Psychiatry

    (2014)
  • C.F. Zink et al.

    Human striatal responses to monetary reward depend on saliency

    Neuron

    (2004)
  • A.T. Beck et al.

    Differentiating anxiety and depression: A test of the cognitive content-specificity hypothesis

    Journal of Abnormal Psychology

    (1987)
  • A.T. Beck

    Depression; causes and treatment

    (1972)
  • A.T. Beck

    The evolution of the cognitive model of depression and its neurobiological correlates

    American Journal of Psychiatry

    (2008)
  • J.S. Beer et al.

    Roles of medial prefrontal cortex and orbitofrontal cortex in self-evaluation

    Journal of Cognitive Neuroscience

    (2010)
  • J.R. Blair et al.

    Predicting premorbid IQ: A revision of the national adult reading test

    Clinical Neuropsychology

    (1989)
  • A.L. Bouhuys et al.

    Depressed patients’ perceptions of facial emotions in depressed and remitted states are associated with relapse: A longitudinal study

    Journal of Nervous and Mental Disease

    (1999)
  • M.L. Brandi et al.

    The neural correlates of planning and executing actual tool use

    Journal of Neuroscience

    (2014)
  • T. Canli et al.

    Brain activation to emotional words in depressed vs healthy subjects

    Neuroreport

    (2004)
  • A.E. Cavanna

    The precuneus and consciousness

    CNS Spectrums

    (2007)
  • G. Dammann et al.

    The self-image in borderline personality disorder: An in-depth qualitative research study

    Journal of Personality Disorders

    (2011)
  • Cited by (42)

    View all citing articles on Scopus
    1

    University of Minnesota, Department of Psychiatry, 2450 Riverside Avenue, Mpls, MN, 55454, USA.

    2

    University of Pittsburgh, School of Public Health, 281 Heather Drive, Pittsburgh, PA,15209, USA.

    3

    University of Pittsburgh Graduate School of Public Health, 130 De Soto Street, Pittsburgh, PA 15261, USA.

    View full text