Neural correlates of decision making and executive function in suicidal thoughts and behaviors

Background: To investigate the neural alterations associated with decision-making (DM) and/or executive function (EF) in psychiatric patients with suicidal thoughts and behaviors (STBs).

Methods: Systematic searches for relevant publications were performed using the PubMed, ScienceDirect and Web of Science databases. A method of quantitative coordinate-based meta-analysis, known as anisotropic effect size version of seed-based d mapping (ASE-SDM), was used to locate brain regions displaying anomalous activations in patients with STBs compared to patient controls (PCs) based on DM and EF tasks, separately. Moreover, we used multimodal analysis to investigate the neural correlates of DM and EF tasks in the brain. Additionally, sensitivity analysis was conducted to assess the robustness of the results, and publication bias was evaluated to ensure the reliability of the findings.

Results: The results pertaining to the DM tasks revealed significant hyper-activations of the left anterior cingulate cortex (BA 24, p = 0.000371) and right insula (p = 0.000640), together with hypo-activations of left insula (p = 0.000387) and left hippocampus (p = 0.0000619) in patients with STB compared to PCs. During the EF tasks, patients with STB only showed hyper-activations in the left anterior cingulate cortex (BA 24, p = 0.00121) and left precentral gyrus (p = 0.00391) compared to PCs. The multimodal analysis elucidates the significance of the cingulate cortex in both DM and EF processes.

Conclusions: Our results suggest that dysregulated neural activity of the ACC is a key mechanism contributing to suicidal risk, with DM abnormalities playing a more central role than EF deficits. These findings highlight potential targets for interventions, such as cognitive-behavioral therapies focusing on DM and impulsivity, or targeting the shared brain region in the left ACC, which could reduce suicidal behavior. Addressing emotional regulation through mindfulness-based therapies may also be beneficial. Future research should validate these interventions and explore their long-term efficacy. This study has been registered in PROSPERO (number CRD42022340922).

1 Introduction

Suicidal thoughts and behaviors (STBs) are not only a personal mental health issue but also a significant public and social health challenge that impacts global economic and social development (1). Despite a growing number of studies to understand the risk factors and mechanisms underlying suicidal behavior the rates of suicide remain high.

Studies of populations at high risk for suicide have showed that STB is linked to impairments in decision making (DM) and executive function (EF) (2), which are two related but different cognitive processes. DM primarily encompasses the prediction, risk assessment, and value judgment of future outcomes, whereas EF pertains to capacity to direct behavior and suppress irrelevant or automatic responses. A substantial body of literature exists relating to study of the biological and psychological factors associated with impaired DM and EF in STB (3, 4). It has been suggested that deficiencies in EF are a common pathway leading to suicidal behavior (5), and deterioration of EF is the principal factor contributing to impaired DM in individuals with depression, significantly influencing the DM process through aspects such as inhibitory control and cognitive flexibility (6). Conversely, some researchers have suggested that impaired DM is the principal factor associated with susceptibility to suicide in individuals (7). The present study has been conceived to shed light on the question of whether deficits in DM or EF have greater influence on STB.

In recent years, numerous studies have investigated the association between suicidal behavior and neurocognitive factors. A meta-analysis conducted by Escobar et al. (8) revealed that, despite absence of significant differences in response time, individuals with a history of suicide attempts exhibited significant deficits in the performance of EF tasks. With regard to individual studies, Gifuni et al. (9) found evidence of deficits in both DM and EF in adolescents who exhibited suicidal behavior, Perrain et al. (10) reported that particularly individuals who have resorted to violent methods of attempted suicide, exhibit a propensity for making higher-risk choices in DM tasks, and Sastre-Buades et al. (7) reported that individuals with suicidal tendencies generally demonstrate poorer performance in DM tasks. Collectively, these studies underscore the critical role of impairments in both DM and EF in suicidal behavior, however whether one is more predominant than the other remains to be elucidated. Functional magnetic resonance imaging (fMRI) is an indispensable advanced neuroimaging technology for assessing cognitive impairment and prefrontal cortex (PFC), especially medial prefrontal cortex (mPFC), consistently emerges as the brain region that is most frequently activated in the performance of DM and EF tasks. Interestingly, alterations in activation of PFC (11, 12), orbitofrontal cortex and amygdala (13) have been reported in individuals with STB during performance of DM tasks, whereas alterations of PFC, (14) basal ganglia and anterior cingulate cortex (ACC) have been reported in individuals with STB during performance of EF tasks (15, 16). While these findings contribute significantly to understanding the neural underpinnings of DM and EF in individuals with STB, results from individual studies often rely on data from small samples which may lead to inconsistencies and low reliability (17). Consequently, in the present study a quantitative meta-analysis of all previous fMRI studies of DM and EF in patients with STB has been performed. Importantly, studies that derived brain areas based on a priori hypothesis have been excluded to avoid potential bias. Additionally, sensitivity and meta-regression analyses have been performed to confirm the accuracy of the findings that are reported.

2 Methods

2.1 Search strategies

A systematic and comprehensive search was conducted in the PubMed, ScienceDirect, and Web of Science databases on Sep 9, 2024 to identify fMRI studies of patients with STB during DM and/or EF task. The following search terms were used: (“suicide” OR “suicidal” OR “suicidality”) AND (“mental processes” OR neuropsychology OR decision-making OR “decision making” OR reward OR “executive function*” OR “cognitive control” OR inhibition OR updating OR shifting OR “working memory”) AND (fMRI OR “functional magnetic resonance imaging”). There was no restriction on the publication date and only original articles published in English were considered, and the reference lists of relevant review papers (18–20) were checked for additional publications related to the topic. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (http://Prisma-statement.org) have been adhered to throughout the present study (Supplementary Table S1), and the study underwent an assessment by PROSPERO (CRD42022340922).

2.2 Selection criteria

Studies were included if they met the following criteria: (i) the patient group included individuals with a history of suicidal ideation and/or suicide attempt (SA), collectively referred to as STB, with no limitation on age, sex and psychiatric comorbidities, (ii) the control group was defined as patients with the same psychiatric disorder as the patient group but without STB in their lifetime, (iii) task-based fMRI had been performed to investigate DM and/or EF, (iv) the control task encompassed all elements of the associated task condition, except for the specific aspect of interest, (v) studies were based on whole-brain analysis, (vi) brain areas were reported as peak coordinates in stereotactic space. Reviews, abstracts, theses, case reports, editorials, letters, and conference proceedings were excluded in the analysis.

2.3 Review selection

Screening of the studies which the search had identified for potential inclusion in the meta-analysis was carried out by TFF and ZL using EndNote X8. Firstly, duplicates were removed. Secondly, unwanted types of literature were excluded by scrutinizing keywords in the titles and abstracts. Thirdly, a thorough examination of the titles and abstracts of the studies to potentially be included was performed to assess relevance. During this process, the full texts of relevant articles was read, with a focus on the Methods section and particular attention paid to the participants that were recruited, MRI that was performed, fMRI tasks used, and statistical analyses that was performed. Studies that met the following criteria were categorized as “possibly included”: (i) patients at a high risk of suicide, including those with STB, (ii) all participants completed a DM and/or EF fMRI task and (iii) regions of brain activation were reported. Studies categorized as “possibly included” underwent further detailed screening until a final decision could be made. For example, if the coordinates of peak activation were not reported the primary author was contacted to request whether this information could be provided.

2.4 Data extract and quality assessment

The following information was compiled for all the studies that were selected for inclusion in the meta-analysis: first author, year of publication, cohort size, demographics (including sex, age, type of suicide and psychiatric diagnosis), task information (including type of task and task performance), imaging parameters (such as magnetic field strength, stereotactic template use and name of analysis software), medication and statistical threshold. Prior to the meta-analysis, the reported peak coordinates of activity and their corresponding t-values were extracted into a text file. During the extraction process, the following considerations were taken into account. Firstly, peak coordinates (x, y, z) reported in Talairach space were converted to MNI space using the ‘tal2icbm_fsl’ transform (http://www.brainmap.org/icbm2tal/), as described by Lancaster et al. (21). Secondly, in cases where statistical significance was reported as a z-value this was converted to a t-value using the Statistics Converter (http://www.sdmproject.com/utilities/?show=Statistics). Thirdly, if no t or z-value was reported, a ‘p’ or ‘n’ (indicating a positive or negative direction of activation, respectively) was chosen as a substitute (22). Finally, once the text files containing the extracted data from all studies had been prepared, a table was created in which each line represents a study and includes the name of the first author, participant sample size and tt statistic. This extraction process was performed by ZL and was subsequently reviewed by TFF.

To assess the quality of individual studies, a checklist based on common elements from existing criteria for assessing psychoradiology studies was used. The checklist, which was tailored to the objectives of the present study, consisted of 10 items organized into three categories, namely participant inclusion, image acquisition and analysis, and results reporting (Supplementary Table S2). The checklist was independently scored by two investigators (TFF and ZL) and any discrepancies were resolved by consensus following discussion.

2.5 Main meta-analysis

2.5.1 Meta-analysis of DM tasks

A coordinate-based meta-analysis based on DM tasks was performed using version 5.15 of the anisotropic effect-size signed differential mapping software (AES-SDM, http://www.sdmproject.com). This software allows for the reconstruction of a 3D statistical image of the regions of brain activation that can be used for group-level analysis. Details of the methods have been described elsewhere (22), and the main steps of the analytic procedure to create the statistical image are as follows. Firstly, peak coordinates were convolved with an anisotropic Gaussian kernel with full width at half maximum (FWHM) of 20 mm, and voxel size of 2 mm within a full brain mask. The choice of full anisotropy (i.e. anisotropy = 1) and FWHM of 20 mm align with standard SDM guidelines and recommendations made by Radua et al. (23) Secondly, the AES-SDM generated Hedges’ effect sizes and their associated variances were computed based on the peak coordinates and t statistics extracted from the original studies by employing standard formulas (22). Thirdly, the peak effect size and Gaussian kernel were utilized to estimate the lower and upper bounds of possible effect sizes for each study. Finally, the most likely effect size and its standard error were estimated for all voxels in the statistical image.

2.5.2 Meta-analysis of EF tasks

Brain activation differences of EF task between patients with STB and PCs were also analyzed with a similar procedure with DM meta-analysis.

2.6 Multimodal overlapping of DM and EF tasks in STB

In this study, to clarify whether DM and EF have the same activation pattern in brain regions in patients with STB. Therefore, we overlapped DM and EF tasks altered regions to examine convergence in results from different task types using the “multimodal” analysis of SDM software with the default option (i.e., to find the regions presenting differences both at the DM and EF task).

2.7 Sensitivity and heterogeneity analyses

A Jack-knife sensitivity analysis, in which one dataset was excluded at a time to determine whether the results remained significant, was performed to assess the reliability of the results. Lastly, the Egger test (24), as implemented in SDM, was used to assess the asymmetry of funnel plots so as to detect any potential publication bias for DM and EF studies, separately.

2.8 Meta-regression and subgroup analyses

Furthermore, meta-regression analyses were performed to examine the potential effects of sex, age and sample size across studies, with these variables serving as predictors and using a threshold of p < 0.0005 for DM and EF studies, separately.

We conducted an additional subgroup analysis of studies of SA and suicide ideation respectively.

3 Results

3.1 Descriptive characteristics and quality assessment of included studies

A total of 14 studies (25–38), comprising 293 patients with STB and 414 PCs, were included in the main meta-analysis (Figure 1). It is worth mentioning that three studies were removed from the list of possibly included studies. Two lacked reported brain coordinates (39, 40), and one (41) involved patients who were immediate biological relatives of individuals who had died by suicide. There were no significant differences in the age of the patients with STB (29.36 ± 15.37 years) and age of the PCs (29.92 ± 16.18 years) (t = -0.10, p = 0.93) nor in their sex (female proportion of 52.21% for patients with STB and 51.93% for PCs, χ² = 0.006, p = 0.94). In total, there are 8 fMRI studies based on DM tasks (performed by 183 patients with STB and 229 PCs) and 6 fMRI studies based on EF tasks (performed by 110 patients with STB and 185 PCs). Thirteen studies were performed using a 3.0 T MRI system and one study used a 1.5 T MRI system. The voxel size of the acquired images ranged from an isotropic voxel size of 2.5 mm to 3.75 mm. Clinical characteristics and demographic information for the participants are presented in Table 1, and task type, analysis software, magnetic field strength, voxel size, threshold, and quality score for each study are presented in Supplementary Table S3 of the Supplementary Materials. Information regarding medication that was being taken by the patients is presented in Supplementary Table S4 of the Supplementary Materials. The mean quality score was 8.5 out of 10 items (range, 7-9.5) (Supplementary Table S3).

Figure 1

Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flowchart.

Table 1

Table 1. Details of the demographic and clinical characteristics of the studies included in the meta-analysis.

3.2 Meta-analysis of DM tasks

During the DM processing, patients with STB showed hyper-activation in left ACC (BA24, p = 0.000371) and right insula (p = 0.000640), and hypo-activation in left insula (BA 48, p = 0.000387) and left hippocampus (Brodmann area 20, p = 0.0000619) compared to PCs (Table 2 and Figure 2).

Table 2

Table 2. Regional differences in activations between patients with STB and patient controls during DM or EF tasks.

Figure 2

Figure 2. Between-group analysis of brain region alteration in patients with STB compared with PCs (A). During DM tasks; (B). During EF tasks; (C). Multimodal analysis combining DM and EF tasks. Red: activation; Blue: deactivation; L, left; R, right; STB, suicide thoughts and behaviors; PCs, Patient controls; DM, Decision making; EF, Executive function.

3.3 Meta-analysis of EF tasks

During the EF processing, patients with STB showed hyper-activation in left ACC (BA24, p = 0.00121) and left precentral gyrus (p = 0.00391) compared to PCs, and no hypo-activated brain regions were found (Table 2 and Figure 2).

3.4 Uniformity analysis of DM and EF tasks

To evaluate the consistent activated abnormal brain regions of the DM and EF tasks, we made a multimodal analysis, and we found that right ACC was increased in DM and EF with good agreement, while left insula was decreased in DM and increased in EF, and no brain regions with decreased activation in DM and EF were found. For enhanced clarity, we have condensed all main outcomes and uniformity analysis findings into Table 3.

Table 3

Table 3. Summary of analysis results.

3.5 Sensitivity analysis and publication bias

Results of the whole-brain jack-knife sensitivity analysis are presented in Supplementary Table S5 of the Supplementary Materials. The brain regions from meta-analysis of DM tasks were more stable than those of EF tasks across study combination. Evidence of publication bias was not found for any of the brain regions for which effects are reported (Supplementary Table S6, p > 0.05).

3.6 Meta-regression and subgroup analyses

Through meta-regression analysis, we did not find any significant effects of mean age and the percentage of female patients in the study cohort. However, the size of the cohort of patients with STB was associated with gray matter activation in left ACC (MNI coordinates: x = 4, y = 30, z = 26, SDM = 1.7, p = ~0) (Figure 3). To assess the impact of sample size, we divided the studies into two groups: those with over 15 participants showed significant ACC activation, while those with 15 or fewer did not. The subgroup analysis suggested that the activation pattern in SI more closely resembles that of the DM task results, though the overall extent of brain impairment appears less pronounced than in the SA subgroup (Table 2).

Figure 3

Figure 3. The meta-regression analysis revealing a significant association between sample size and brain activation in the right anterior cingulate cortex.

4 Discussion

Understanding the neuropsychological mechanisms underlying DM and EF processes in patients with STB is crucial for effective risk assessment and intervention strategies. Establishing a cohesive framework that integrates DM and EF is crucial for interpreting the study’s findings. Moreover, a detailed examination of distinct regional contributions remains essential for a comprehensive understanding of the underlying neural mechanisms. For example, the ACC is a commonly activated area implicated in both cognitive functions. Although the left insula does not exhibit significant activation in EF, our multimodal analysis reveals that it is an abnormal brain region shared by the two tasks.

4.1 Altered neural circuitry across DM and EF tasks

In this study, we identified altered neural activity in STB patients in ACC was implicated in both DM and EF, suggesting a shared neurocognitive disruption. The left ACC and right insula exhibited hyperactivation in DM task, which forms key nodes of the Salience Network (42). During DM, hyperactivation in these regions suggests heightened sensitivity to negatively valenced information and impaired assessment of positive outcomes, potentially leading to altered risk perception and preferential engagement in avoidance behaviors (43). Conversely, hypoactivation in the Default Mode Network, i.e., left insula and hippocampus may reflect disorganized affective integration and contextual memory retrieval, further compromising adaptive DM (44).

Concurrently, we observed increased activation in the ACC and precentral gyrus during EF tasks, indicating enhanced effort toward impulse control in patients with STB, compared with patient controls (42). This common ACC engagement across both domains’ points to its central role in monitoring conflict and regulating emotional and cognitive responses.

The hyperactivation in Salience Network and suppression of Default Mode Network activity suggest a persistently alert, control-oriented cognitive state—even long after the STB episode—which may reflect enduring difficulties in disengaging from threat-related processing and adjusting behavioral responses, supporting these stable aberrations in regions is a potential neurobiological trait marker of STB.

4.2 Role of anterior cingulate gyrus in DM and EF tasks

Our study found that the left ACC was hyperactivated while STB patients performing the DM and EF tasks. The ACC plays a pivotal role in EF and DM processes, particularly during complex cognitive tasks and emotional feedback processing (45, 46). Neuroimaging studies have revealed distinct activation patterns in the ACC across varying psychological states and task conditions, providing critical insights into the cognitive-emotional mechanisms of STB. For example, research demonstrates that suicide attempters exhibit functional abnormalities in the prefrontal cortex and cingulate gyrus during DM tasks, potentially impairing their capacity for reward-based DM under emotional contexts (47). These dysfunctions may correlate with hyperactivation of the ACC during emotional information processing and executive control (48). Moreover, the ACC shows altered functional connectivity with other key brain regions during these processes. For instance, ACC-orbitofrontal cortex synchronization plays an essential role in value-guided DM, with enhanced coupling observed during high-reward selections (49). Such connectivity disturbances may underlie the DM impairments characteristic of suicide attempters (50). In summary, the observed ACC hyperactivity during EF and DM tasks likely reflects core cognitive-emotional dysregulation in STB (51). Further investigation of state-dependent ACC functional dynamics could advance our understanding of suicidal neuropathology and inform novel clinical interventions.

In prior research abnormalities in mPFC have been reported in patients with psychiatric disorders associated with suicide risk, such as major depressive disorder and bipolar disorder (52). In addition, Prior research undertaken by our team (53) in which increased activation of mPFC was reported in patients with alcohol use disorder during response inhibition tasks, aligns with the findings of the present study. However, this study did not find the impaired activation in the above brain regions. Further exploration is needed to determine whether these regions are critically implicated in suicide risk through whole-brain studies.

4.3 Impairment of hippocampus during DM tasks

The significant hypo-activation of left hippocampus in patients with STB compared to PCs when performing DM tasks, was not observed for EF task, suggesting that there may be a distinct neural signature associated with DM processes in individuals with a history of STB (54). The hippocampus plays a crucial role in guiding the selection of appropriate DM strategies (55–57). This observation is in line with a prior review highlighting the importance of enhancing cognitive functions involving the hippocampus for effective suicide prevention (58). Beyond its functional role, the hippocampus has been implicated in psychopathological changes associated with suicide, whereby the heightened sensitivity of the hippocampus to stress represents a notable risk factor contributing to STB (59).

The fact that hypo-activation of the hippocampus was not observed during EF tasks points to a task-specific deficit rather than a global reduction in neural activity and suggests that cognitive impairments in patients with STB may be domain-specific (60). This finding is consistent with prior research showing that cognitive impairments in suicide attempters tend to be more pronounced in tasks requiring higher-order cognitive abilities (8).

4.4 Roles of insula in DM tasks

The meta-analysis has revealed there to be significantly dysregulated in insula activation patterns between patients with STB and PCs during performance of DM tasks. The bilateral insula has been reported to play a crucial role in processing of negative emotions, interoceptive awareness and risk assessment (61). Increased activation in the right insula during DM tasks has been suggested to reflect heightened emotional reactivity and difficulty in processing negative emotional stimuli, potentially contributing to impulsivity and risky DM (62). The left insula is closely related to positive emotions (63), and impaired activation in this brain area during the DM task in patients with STB suggests that the response to potential rewards is weakened, affecting the motivation of DM (64).

In addition, our multimodal analysis also found that in DM, left insula also showed a new result, namely that this brain region also increased activation in EF. As a new result in the multimodal analysis, we need to be cautious about this result, although studies show that the left insula can participate in the dynamic regulation of executive functional networks through functional connectivity with other brain regions (e. g., prefrontal cortex, anterior cingulate, and parietal cortex) (65).

4.5 Role of precentral cortex in EF tasks

The current study identified increased activation in the precentral gyrus during EF tasks, aligning with the dual role of the precentral cortex in motor planning and higher cognitive functions (66). While it is a critical component of the primary motor cortex, the precentral cortex also engages in cognitive control, response inhibition, and attentional regulation through its functional connectivity with the prefrontal cortex (67). Neuroimaging studies indicate that the precentral cortex collaborates with the prefrontal cortex during EF tasks to convert cognitive control signals into motor outputs, particularly in scenarios requiring rapid response inhibition and task switching (68). Additionally, as a pivotal node in the mirror neuron system (69), the precentral cortex may further support its involvement in higher cognitive functions, such as theory of mind and empathy. Impairment of this region may result in deficits in EF, particularly in motor planning and cognitive control tasks (70). These findings underscore the significance of the precentral cortex within EF networks, offering new insights into its role in prefrontal-motor cortical circuits (71).

4.6 Limitations

While providing novel insights, this meta-analysis has several important limitations that warrant cautious interpretation of the findings: First, our reliance on reported peak coordinates and effect sizes (rather than raw statistical maps) inherently reduces spatial precision and may obscure subtle but clinically relevant neural patterns. This methodological approach, while common in neuroimaging meta-analyses, prevents more nuanced characterization of neural circuitry. Second, the inclusion of patients with varied comorbid psychiatric disorders introduces important clinical heterogeneity. This diversity in psychiatric comorbidities may have potentially obscured suicide-related neural features that are independent of primary diagnoses. These inherent clinical variations suggest our findings likely reflect shared transdiagnostic vulnerabilities to suicidal behavior across psychiatric disorders rather than suicide-specific neural markers. Third, the cross-sectional nature of included studies fundamentally limits causal inference regarding whether the observed neural alterations represent predisposing vulnerabilities or consequences of suicidal states. Longitudinal designs with repeated assessments will be crucial for disentangling these temporal relationships.

5 Conclusions

This meta-analysis reveals distinct neural patterns in STB patients, with DM-related regions showing hypoactivation—indicating impaired reward and risk processing—and DM/EF-related regions exhibiting hyperactivation, which may reflect compensatory efforts or increased cognitive demand. As a common activated region in both DM and EF tasks, the cingulate gyrus emerges as a key hub linking these domains, underscoring its role in integrating these two cognitive processes. These dysfunctions may underlie the core pathophysiology of DM and EF deficits in patients with a history of STB.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Ethics statement

Ethical approval was not sought as the data retrieved and analyzed for this research were obtained from previous studies where informed consent was already obtained by the primary investigators.

Author contributions

FT: Data curation, Software, Validation, Visualization, Writing – original draft. LZ: Data curation, Investigation, Methodology, Software, Writing – original draft. XL: Formal analysis, Validation, Writing – review & editing. NR: Formal analysis, Methodology, Writing – review & editing. HP: Conceptualization, Funding acquisition, Project administration, Supervision, Writing – review & editing.

Funding

The author(s) declare financial support was received for the research and/or publication of this article. This study was supported by the National Natural Science Foundation (Grant No. 82472019) and the China Postdoctoral Science Foundation (Grant No. 0303020201P0613).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Generative AI statement

The author(s) declare that no Generative AI was used in the creation of this manuscript.

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Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpsyt.2025.1676986/full#supplementary-material

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