Reward Versus Nonreward Sensitivity of the Medial Versus Lateral Orbitofrontal Cortex Relates to the Severity of Depressive Symptoms

Xie, Chao; Jia, Tianye; Rolls, Edmund T.; Sahakian, Barbara J.; Zhang, Jie; Liu, Zhaowen; Cheng, Wei; Luo, Qiang; Lo, Chun-Yi Zac; Wang, He; Banaschewski, Tobias; Barker, Gareth; Bokde, Arun L.W.; Büchel, Christian; Quinlan, Erin Burke; Desrivières, Sylvane; Flor, Herta; Grigis, Antoine; Garavan, Hugh; Gowland, Penny; Heinz, Andreas; Hohmann, Sarah; Ittermann, Bernd; Martinot, Jean‐Luc; Martinot, Marie‐Laure Paillère; Nees, Frauke; Orfanos, Dimitri Papadopoulos; Paus, Tomáš; Poustka, Luise; Fröhner, Juliane H.; Smolka, Michael N.; Walter, Henrik; Whelan, Robert; Schumann, Günter; Feng, Jianfeng; Artiges, Éric; Aydın, Semiha; Barbot, Alexis; Becker, Andreas; Bézivin-Frere, Pauline; Biondo, Francesca; Chu, Congying; Conrod, Patricia J.; Daedelow, Laura S.; Dalley, Jeffrey W.; Dooley, Eoin; Filippi, Irina; Fillmer, Ariane; Frouin, Vincent; Grimmer, Yvonne; Ihlenfeld, Albrecht; Ing, Alex; Isensee, Corinna; Lemaître, Hervé; Lethbridge, Emma; Millenet, Sabina; Miller, Sarah; Miranda, Rubén; Paillère, Marie-Laure; Papadopoulos, Dimitri; Pausová, Zdenka; Pentilla, Jani; Poline, Jean‐Baptiste; Burke, Erin; Rapp, Michael A.; Robbins, Trevor W.; Robert, Guillaume; Rogers, John; Ruggeri, Barbara; Stringaris, Argyris; Noort, Betteke van; Simon, Roux; Williams, Steve; Zhang, Yuning

doi:10.1016/j.bpsc.2020.08.017

Cited by 34 publications

(47 citation statements)

References 44 publications

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“…1 ) is activated by rewarding and subjectively pleasant stimuli and has reduced functional connectivity in depression. This difference is supported by recent investigations in, for example, a monetary Win versus NoWin task ( Xie et al , 2020 ).…”

Section: Introductionsupporting

confidence: 66%

“…In humans, the medial OFC is activated by many rewarding stimuli and reflects their subjective pleasantness ( Grabenhorst and Rolls, 2011 ; Rolls, 2019c ). This is found for odours ( Rolls et al , 2003a ), flavour ( de Araujo et al , 2003 ; Kringelbach et al , 2003 ), pleasant touch ( Rolls et al , 2003b ; McCabe et al , 2008 ), monetary reward ( O’Doherty et al , 2001 ; Xie et al , 2020 ) and amphetamine ( Völlm et al , 2004 ). A recent study with 1877 participants emphasizes these points, by showing that the medial OFC is activated by reward (such as winning money or candies) and that the lateral OFC is activated by not winning ( Fig.…”

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 80%

“…The interaction term showing the sensitivity of the medial OFC to reward and the lateral OFC to non-reward was significant at P = 10 −50 at age 19 and P < 10 −72 at age 14. In a subgroup with depressive symptoms as shown by the Adolescent Depression Rating Scale, it was further found that there was a greater activation to the No Win condition in the lateral OFC; and the medial OFC was less sensitive to the differences in reward value (modified from Xie et al , 2020 ).…”

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 95%

“…A recent study with 1877 participants emphasizes these points, by showing that the medial OFC is activated by reward (such as winning money or candies) and that the lateral OFC is activated by not winning ( Fig. 5 ) ( Xie et al , 2020 ). Humans with OFC lesions may also be less sensitive to reward, as shown by their reduced subjective emotional feelings and altered social and emotional behaviour and problems with face and voice expression processing ( Rolls et al , 1994 ; Hornak et al , 1996 , 2003 ; Rolls, 2021b ).…”

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 95%

“…Neuroimaging experiments in humans (‘Technical Note’) produce consistent evidence about reward value representations ( de Araujo et al , 2003 ; Kringelbach and Rolls, 2003 ; Kringelbach et al , 2003 ; Grabenhorst and Rolls, 2008 ; Grabenhorst et al , 2008a ), and allow the types of reward to be extended to include monetary reward ( O’Doherty et al , 2001 ; Xie et al , 2020 ), face expressions ( Kringelbach and Rolls, 2003 ) and face beauty ( O’Doherty et al , 2003 ). In humans, the medial OFC is activated by many rewarding stimuli and reflects their subjective pleasantness ( Grabenhorst and Rolls, 2011 ; Rolls, 2019c ).…”

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 99%

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The orbitofrontal cortex: reward, emotion and depression

Rolls

Cheng

Feng

2020

Brain Communications

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266

148

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The orbitofrontal cortex in primates including humans is the key brain area in emotion, and in the representation of reward value and in non-reward, that is not obtaining an expected reward. Cortical processing before the orbitofrontal cortex is about the identity of stimuli, i.e. ′what′ is present, and not about reward value. There is evidence that this holds for taste, visual, somatosensory, and olfactory stimuli. The human medial orbitofrontal cortex represents many different types of reward, and the lateral orbitofrontal cortex represents non-reward and punishment. Not obtaining an expected reward can lead to sadness, and feeling depressed. The concept is advanced that an important brain region in depression is the orbitofrontal cortex, with depression related to over-responsiveness and over-connectedness of the non-reward-related lateral orbitofrontal cortex, and to under-responsiveness and under-connectivity of the reward-related medial orbitofrontal cortex. Evidence from large-scale voxel-level studies and supported by an activation study is described that provides support for this hypothesis. Increased functional connectivity of the lateral orbitofrontal cortex with brain areas that include the precuneus, posterior cingulate cortex, and angular gyrus is found in patients with depression, and is reduced towards the levels in controls when treated with medication. Decreased functional connectivity of the medial orbitofrontal cortex with medial temporal lobe areas involved in memory is found in patients with depression. Some treatments for depression may act by reducing activity or connectivity of the lateral orbitofrontal cortex. New treatments that increase activity or connectivity of the medial orbitofrontal cortex may be useful for depression. These concepts, and that of increased activity in non-reward attractor networks, have potential for advancing our understanding and treatment of depression. The focus is on the orbitofrontal cortex in primates including humans, because of differences of operation of the orbitofrontal cortex, and indeed of reward systems, in rodents. Finally, the hypothesis is developed that the orbitofrontal cortex has a special role in emotion and decision-making in part because as a cortical area it can implement attractor networks useful in maintaining reward and emotional states online, and in decision-making.

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Section: Introductionsupporting

confidence: 66%

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 80%

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 95%

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 95%

Section: The Orbitofrontal Cortex Is a Key Brain Region In Reward Valmentioning

confidence: 99%

See 3 more Smart Citations

The orbitofrontal cortex: reward, emotion and depression

Rolls

Cheng

Feng

2020

Brain Communications

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266

148

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Emotion, motivation, decision-making, the orbitofrontal cortex, anterior cingulate cortex, and the amygdala

Rolls

2023

Brain Struct Funct

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The orbitofrontal cortex and amygdala are involved in emotion and in motivation, but the relationship between these functions performed by these brain structures is not clear. To address this, a unified theory of emotion and motivation is described in which motivational states are states in which instrumental goal-directed actions are performed to obtain rewards or avoid punishers, and emotional states are states that are elicited when the reward or punisher is or is not received. This greatly simplifies our understanding of emotion and motivation, for the same set of genes and associated brain systems can define the primary or unlearned rewards and punishers such as sweet taste or pain. Recent evidence on the connectivity of human brain systems involved in emotion and motivation indicates that the orbitofrontal cortex is involved in reward value and experienced emotion with outputs to cortical regions including those involved in language, and is a key brain region involved in depression and the associated changes in motivation. The amygdala has weak effective connectivity back to the cortex in humans, and is implicated in brainstem-mediated responses to stimuli such as freezing and autonomic activity, rather than in declarative emotion. The anterior cingulate cortex is involved in learning actions to obtain rewards, and with the orbitofrontal cortex and ventromedial prefrontal cortex in providing the goals for navigation and in reward-related effects on memory consolidation mediated partly via the cholinergic system.

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