Large-scale neural network computations and multivariate representations during approach-avoidance conflict decision-making

Moughrabi, Nicole; Botsford, Chloe; Gruichich, Tijana Sagorac; Azar, Ameera; Heilicher, Mickela; Hiser, Jaryd; Crombie, Kevin M.; Dunsmoor, Joseph E.; Stowe, Zach; Cisler, Josh M.

doi:10.1016/j.neuroimage.2022.119709

Cited by 8 publications

(14 citation statements)

References 88 publications

(128 reference statements)

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“…In accordance with prior research, we found that when making approach-avoidance decisions, individuals balance potential rewards and threats against each other (Talmi et al, 2009; Basten et al, 2010; Park et al, 2011; Aupperle et al, 2015; Schlund et al, 2016; Hulsman et al, 2021a, 2024; Klaassen et al, 2021; Moughrabi et al, 2022). Subsequently, we employed Bayesian Multivariate Multilevel (BMM) analyses to delve deeper into the specific contributions of regions traditionally associated with reward and threat processing to approach-avoidance decision-making under these mixed outcome prospects.…”

Section: Discussionsupporting

confidence: 90%

“…The observed integration patterns of reward and threat notably diverge from prior human imaging research, which indicated such integration primarily in cortical regions such as the dACC, dlPFC, dmPFC, and inferior frontal gyrus (Basten et al, 2010; Park et al, 2011; Zorowitz et al, 2019; Moughrabi et al, 2022). Our findings of subcortical integration, therefore provide a new perspective although they do resonate with other previous non-human literature (Costa et al, 2016; Gentry et al, 2016; Burgos-Robles et al, 2017; Hamel et al, 2017).…”

Section: Discussioncontrasting

confidence: 89%

“…Furthermore, the observed increase in threat-related activity in the vStriatum, thalamus, and BNST preceding avoidance relative to approach under low reward, aligns with recent findings that increased threat representations in these regions during decision-making were linked to avoidance (Moughrabi et al, 2022). Behaviourally, the presence of high reward attenuated the impact of threat on subsequent decisions.…”

Section: Discussionsupporting

confidence: 86%

“…Moreover, recent rodent studies have shown that subcortical regions, including the central nucleus of the amygdala (CeA) and nucleus accumbens (NAcc) can trigger both approach and avoidance motivation depending on the context and input received from other structures (Warlow et al, 2020; Zhou et al, 2022) and that regions of the thalamus respond particularly to situations requiring integration, such as approach-avoidance conflict (Engelke et al, 2021). This aligns with recent human work showing that regions of the salience network (thalamus, periaqueductal gray, dACC, and anterior insula) are sensitive to both rewards and threats (Aupperle et al, 2015; Schlund et al, 2016; Moughrabi et al, 2022). Strikingly, however, none of the aforementioned human studies investigated how the interplay between reward and threat is represented across these brain regions and how this balance shifts upon decisions to approach or avoid.…”

Section: Introductionsupporting

confidence: 91%

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How distributed subcortical integration of reward and threat may inform subsequent approach-avoidance decisions

Hulsman,

Klaassen,

de Voogd

et al. 2024

Preprint

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Healthy and successful living involves carefully navigating rewarding and threatening situations by balancing approach and avoidance behaviours. Excessive avoidance to evade potential threats often leads to forfeiting potential rewards. However, little is known about how reward and threat information is integrated neurally to inform either approach or avoidance decisions. In this preregistered study, participants (N=31, 17F) made approach-avoidance decisions under varying reward (monetary gains) and threat (electrical stimulations) prospects during functional MRI scanning. In contrast to theorized parallel subcortical processing of reward and threat information before cortical integration, Bayesian Multivariate Multilevel analyses revealed subcortical reward and threat integration prior to indicating approach-avoidance decisions. This integration occurred in the ventral striatum, thalamus, and bed nucleus of the stria terminalis (BNST). When reward was low, avoidance decisions dominated, reflected in stronger reactivity to threat prior to indicating avoidance decisions across these regions. In addition, the amygdala exhibited dual sensitivity to reward and threat. While anticipating the outcome of approach decisions, characterized by elevated risk of electrical stimulation, increased threat-related activity within the salience network (dorsal anterior cingulate cortex, thalamus, periaqueductal gray, BNST) was observed. Conversely, anticipating the outcome of avoidance decisions, marked by reduced reward potential, was associated with suppression of reward-related activity in the ventromedial prefrontal cortex and ventral striatum. These findings shed light on the temporal dynamics of approach-avoidance decision-making. Importantly, they demonstrate the role of subcortical integration of reward and threat information in balancing approach and avoidance, challenging theories positing predominantly separate subcortical processing before cortical integration.

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Section: Discussionsupporting

confidence: 90%

Section: Discussioncontrasting

confidence: 89%

Section: Discussionsupporting

confidence: 86%

Section: Introductionsupporting

confidence: 91%

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How distributed subcortical integration of reward and threat may inform subsequent approach-avoidance decisions

Hulsman,

Klaassen,

de Voogd

et al. 2024

Preprint

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“…Figure 1b provides an overview of the analytical approach, which is in direct accord with our previous MVPA investigation of prospective representations of reward and threat as a mechanism of decision-making (Moughrabi et al, 2022). The first step was to demonstrate that network activity patterns at the time of reward delivery could accurately be decoded.…”

Section: Multivariate Pattern Analyses Of Prospective Mental Represen...mentioning

confidence: 80%

Diminished prospective mental representations of reward mediate reward learning strategies among youth with internalizing symptoms

Cisler

Tamman

2023

Psychol. Med.

Self Cite

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Background Adolescent internalizing symptoms and trauma exposure have been linked with altered reward learning processes and decreased ventral striatal responses to rewarding cues. Recent computational work on decision-making highlights an important role for prospective representations of the imagined outcomes of different choices. This study tested whether internalizing symptoms and trauma exposure among youth impact the generation of prospective reward representations during decision-making and potentially mediate altered behavioral strategies during reward learning. Methods Sixty-one adolescent females with varying exposure to interpersonal violence exposure (n = 31 with histories of physical or sexual assault) and severity of internalizing symptoms completed a social reward learning task during fMRI. Multivariate pattern analyses (MVPA) were used to decode neural reward representations at the time of choice. Results MVPA demonstrated that rewarding outcomes could accurately be decoded within several large-scale distributed networks (e.g. frontoparietal and striatum networks), that these reward representations were reactivated prospectively at the time of choice in proportion to the expected probability of receiving reward, and that youth with behavioral strategies that favored exploiting high reward options demonstrated greater prospective generation of reward representations. Youth internalizing symptoms, but not trauma exposure characteristics, were negatively associated with both the behavioral strategy of exploiting high reward options as well as the prospective generation of reward representations in the striatum. Conclusions These data suggest diminished prospective mental simulation of reward as a mechanism of altered reward learning strategies among youth with internalizing symptoms.

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Cognitive Signatures of Depressive and Anhedonic Symptoms and Affective States Using Computational Modeling and Neurocognitive Testing

Ging-Jehli,

Kuhn,

Blank

et al. 2024

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

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Large-scale neural network computations and multivariate representations during approach-avoidance conflict decision-making

Cited by 8 publications

References 88 publications

How distributed subcortical integration of reward and threat may inform subsequent approach-avoidance decisions

How distributed subcortical integration of reward and threat may inform subsequent approach-avoidance decisions

Diminished prospective mental representations of reward mediate reward learning strategies among youth with internalizing symptoms

Cognitive Signatures of Depressive and Anhedonic Symptoms and Affective States Using Computational Modeling and Neurocognitive Testing

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