The task’s difficulty was modulated by adjusting the coherence level, representing the strength of the stimulus or motion coherence.
Figure 1B illustrates the random dot kinematogram (RDK) stimulus employed in the RDM experiment, featuring a field of dots, with a certain percentage moving coherently in one direction (signal dots), while the remainder moved randomly (noise dots). Various coherence levels were depicted, with higher coherence indicating a larger proportion of signal dots, facilitating easier perception of motion direction (Newsome & Pare, 1988). The experiment utilized the Psychophysics Toolbox and MATLAB for stimulus control, with EyeLink by SR-Research tracking eye movements.
The training trial structure was as follows: Each trial began with the subject fixating on a small red circle (0.3° diameter) at the screen center. After a delay (200-500 ms; truncated exponential), two red targets (0.5°) appeared equidistant from the fixation point (8° eccentricity). Subsequently, a dynamic random dots stimulus appeared within a 5° circular aperture centered on the fixation point after another random delay (200-500 ms; truncated exponential). The dots were white 4×4-pixel squares (0.096° × 0.096°) on a black background, with a density of 16.7 dots per square degree per second (
Figure 1A). After the motion stimulus offset, a delay period (400-1000 ms; truncated exponential) preceded the fixation point offset. Subjects were instructed to maintain gaze on the fixation point until its offset. Deviation exceeding 2° aborted the trial. Subjects reported the perceived motion direction by shifting gaze to the chosen target and maintaining gaze within 3° for 200 ms. Correct responses received positive feedback, while incorrect responses received negative feedback. The RDM task has been introduced in a previous study (Shadlen & Newsome, 2001). The training continued until subjects achieved high performance (thresholds <17%).
The main experiment focused on simultaneous low- and high-level decision-making, depicted in
Figure 1C. Following motion direction discrimination training, subjects transitioned to the changing environment task (
Figure 1C). The experimental setup, motion stimulus, and event timing were consistent with the training protocol, but subjects were presented with two pairs of choice targets (four targets total) positioned above and below the fixation point (FP) at 10° eccentricities (±3.5° above/below FP; ±9.4° left/right of FP). Each pair of targets represented right and left motion directions, with the upper and lower pairs indicating two distinct environments. For example, selecting the top-left target (
Figure 1C) indicated recognition of leftward dot motion and an upward environmental orientation.
The hierarchical task paradigm began with a small red fixation point at the screen’s center (
Figure 1C). Subjects were required to focus on the red fixation point for approximately 200 ms, and if their gaze deviated by more than 2°, the trial was aborted. Following a random delay (ranging from 200 to 500 ms, obtained from a truncated exponential distribution), two pairs of targets appeared on the screen. The horizontal targets indicated the environmental orientation—whether upward or downward (
Figure 1C). After an additional random delay (again ranging from 200 to 500 ms, obtained from a truncated exponential distribution), dot motion ensued. The duration of dot motion varied randomly, selected from a truncated exponential distribution (ranging from 100 to 900 ms with a mean of 330 ms) for each trial. According to a truncated geometric distribution, the environment remained constant for several trials (ranging from 2 to 15 trials with a mean of 6). At intervals, without warning, the environment changed, prompting subjects to adjust their strategies. Subjects reported their responses—including the direction of RDM, and the environment by fixating on one of the targets and maintaining their gaze for 200 ms using saccadic eye data. This report was based on the history of feedback, choice, and confidence of choice related to several prior trials. Subjects received feedback following the announcement of their decision. Two audible tones were utilized to communicate decision feedback to the subjects, with 250 Hz denoting a correct answer and 1000 Hz indicating an incorrect one. Positive feedback was given when both low- and high-level decisions were correct; negative feedback was given otherwise. In both training phase and main experiment, the dot motion featured six different coherence levels (0%, 3.2%, 6.4%, 12.8%, 25.6%, 51.2%), and trials featuring 0% coherence were randomly selected from a uniform distribution for their motion direction. The experimental paradigm was inspired by previous research (Purcell & Kiani, 2016). Each subject went through 4 to 8 blocks in a session, with each block comprising 200 trials. Out of 16,800 trials, 1,100 trials were excluded.
Recording, preprocessing, and analysis of EEG signals
EEG data were recorded concurrently with eye tracking throughout the experiment. Participants were seated in a semi-darkened, electrically shielded room at a viewing distance of 57 cm from a 17-inch CRT monitor (PF790; 75 Hz refresh rate, 800×600 resolution). Continuous EEG was acquired using a 32-channel amplifier (eWave, Science Beam) from 31 scalp electrodes positioned according to the international 10–20 system (Fp1, Fp2, F3, F4, C3, C4, P3, P4, O1, O2, F7, F8, T3, T4, T5, T6, Fz, Cz, Pz, FC3, FC4, CP3, CP4, FT7, FT8, TP7, TP8, Oz). Signals were referenced online to the right mastoid, with the left mastoid serving as ground. Data were sampled at 1000 Hz, and electrode impedances were kept below 10 kΩ.
Offline preprocessing was performed using EEGLAB and custom MATLAB scripts. Continuous data were band-pass filtered between 0.1 and 35 Hz using a zero-phase Butterworth filter, followed by a 50 Hz notch filter to remove line noise. Ocular and muscular artifacts were corrected using independent component analysis (ICA) with the ADJUST plugin for automatic component classification (Mognon et al., 2011). Bad channels were identified by visual inspection and interpolated using spherical spline interpolation.
For FRN analysis, the cleaned EEG data were segmented into epochs time-locked to feedback onset, spanning from −100 to 500 ms. Baseline correction was applied using the −100 to 0 ms pre-feedback interval. Epochs containing residual artifacts exceeding ±100 µV were automatically rejected.
To characterize the temporal dynamics of the FRN, the post-feedback interval was divided into consecutive, non-overlapping 100-ms windows (0–100, 100–200, 200–300, 300–400, and 400–500 ms). Within each window, the mean ERP amplitude at frontocentral electrodes was computed and statistically compared across experimental conditions using the Kruskal–Wallis test. The FRN was operationally defined as the mean amplitude within the time window exhibiting the strongest negative deflection and significant condition effects. The peak latency of the FRN was identified within this window for descriptive purposes only.
FRN amplitudes were quantified at a cluster of frontocentral electrodes (F3, F4, Fz, Cz), consistent with the canonical scalp distribution of this component (Pfabigan et al., 2015; Wang et al., 2020a). For each participant and experimental condition, FRN amplitude was calculated by averaging across all valid trials. Grand-averaged ERP waveforms revealed a robust negative deflection following negative feedback, replicating the characteristic morphology of the FRN (Oliveira et al., 2005; Wang et al., 2020a) and supporting the validity of the preprocessing and analysis pipeline.
Statistical analysis
All statistical analyses were conducted in MATLAB (R2021b, MathWorks Inc.). The Shapiro-Wilk test was used to assess normality, and as most behavioral and electrophysiological data violated this assumption (P<0.05), non-parametric tests were employed. Data are presented as Mean±SEM, and effect sizes are reported for all significant results.
For behavioral analyses examining the effects of stimulus coherence and feedback history on strategy switching, the Kruskal-Wallis H test was used for comparisons across three or more conditions (e.g. switching probability after 1, 2, or 3 consecutive errors), with significant main effects followed by Dunn’s post-hoc tests and Bonferroni correction. Paired comparisons (e.g. switching after negative vs positive feedback) were performed using the Wilcoxon signed-rank test.
For electrophysiological data, FRN amplitude was analyzed according to our three primary hypotheses. The effect of stimulus strength was tested by comparing FRN amplitudes between high- and low-coherence negative feedback trials using a Wilcoxon rank-sum test. The effect of consecutive negative feedback was assessed by comparing FRN amplitudes following the first, second, and third consecutive errors (pre-switch) with the Kruskal-Wallis H-test and Dunn’s post-hoc tests. The effect of decision urgency was evaluated by comparing FRN amplitudes from trials categorized by their proximity to a strategy switch (distant: 7–9 trials before; intermediate: 4–6 before; immediate: 1–3 before) using the Kruskal-Wallis H test and Dunn’s post-hoc test. Additionally, a Wilcoxon signed-rank test was used to compare FRN amplitude in the trial immediately preceding a switch to that in the trial immediately following it.
For all EEG analyses involving multiple comparisons, P-values were adjusted using the false discovery rate (FDR) correction (Benjamini-Hochberg procedure, α=0.05), and all reported FRN P-values are FDR-corrected. Functional connectivity, analyzed via Pearson correlation between electrode time series in the FRN window, was compared across conditions for key electrode pairs (e.g. Fz–Cz) using Wilcoxon signed-rank tests with FDR correction. Effect sizes are reported as eta-squared (η²) for Kruskal-Wallis tests and rank-biserial correlation (r) for Wilcoxon tests. All tests were two-tailed, with significance set at P<0.05 after FDR correction where applicable.
Results
Behavioral data analysis
We first examined the behavioral data to determine how the three key parameters of hierarchical decision-making—stimulus strength (a proxy for low-level confidence) (Kiani & Shadlen, 2009), the sequence of consecutive negative feedback, and decision urgency—guide strategic switching in a dynamic environment. Our results align with established findings (Purcell & Kiani, 2016a), confirming the validity of our experimental approach.
Initial analyses focused on the psychophysical properties of the task. Consistent with known principles, perceptual accuracy improved as stimulus strength (coherence) increased. This relationship was formalized by fitting a cumulative Weibull function to the choice data (Quick, 1974), providing psychophysical thresholds (α) and slopes (β) for each participant (
Figure 2A) (Zylberberg et al., 2016).
This pre-switch FRN intensification likely reflects heightened error-monitoring activity and increased cognitive effort dedicated to evaluating ongoing performance and initiating corrective behavioral change. The topographic distribution of this enhanced negativity was centered over frontal-central regions, with maximal amplitude at the Fz and Cz electrodes (
Figure 6B), implicating the medial frontal cortex in this preparatory process.
Supporting this interpretation, functional connectivity analysis revealed significantly stronger correlations within a frontal-central network (F3, F4, Fz, and Cz) during pre-switch trials compared to post-switch trials (
Figures 6C and 6D). The mean connectivity strength among these key electrodes was 0.53±0.08 in pre-switch trials versus 0.39±0.07 in switch trials (t-test: P=0.034), indicating more synchronized activity within this network prior to strategic change.
In summary, the convergence of amplitude, topography, and connectivity data demonstrates that FRN modulation serves as a predictive neural signal of impending strategy shifts. The component’s sensitivity to the pre-switch context underscores its role not merely as a feedback evaluator but as an integral part of a proactive system that monitors decision efficacy and mobilizes adaptive resources in anticipation of necessary behavioral change within hierarchical decision-making frameworks.
Discussion
The present study provides a detailed examination of the FRN as a neural correlate of hierarchical decision-making in humans, integrating behavioral and electrophysiological evidence within a single experimental framework. Behavioral analyses showed that negative feedback—particularly when weighted by low-level decision certainty and accumulated across consecutive trials—increases the likelihood of high-level strategy switching (
Figures 2B, 2C, and
2D). These findings underscore the need for active inference to disambiguate the source of negative outcomes, whether arising from inappropriate high-level strategies or unreliable low-level decision execution. However, behavioral measures alone were insufficient to reliably predict the timing of strategy switches, motivating the investigation of neural signals that may reflect latent evaluative processes preceding overt behavioral change.
FRN analyses yielded three main findings. First, FRN amplitude increased systematically with consecutive negative feedback (
Figure 4A), indicating sensitivity to the accumulation of evidence signaling potential strategy failure. Second, FRN enhancement was most pronounced immediately prior to high-level strategy switches (
Figure 6A), suggesting that this signal reflects internal evaluative processes that precede explicit behavioral updating. Third, FRN modulation scaled with stimulus strength and decision urgency (
Figures 3 and
5A), consistent with the integration of low-level decision certainty and higher-order contextual variables. Together, these results suggest that the FRN reflects hierarchical evidence integration processes rather than encoding feedback valence alone.
Importantly, FRN dynamics provided information beyond behavior alone. While behavioral measures capture the outcome of decision processes, FRN fluctuations tracked trial-by-trial changes in internal belief updating that preceded observable strategy switches. In this sense, the FRN appears closely related to a latent decision variable reflecting the accumulation of negative evidence toward a strategy-switch threshold, consistent with computational models of hierarchical decision-making. It is important to note that FRN analyses were primarily restricted to negative feedback trials, in line with the evaluative nature of this component. While urgency-related behavioral analyses incorporated both positive and negative feedback to capture overall decision dynamics, interpretations of FRN modulations are confined to evaluative contexts following negative feedback.
The FRN exhibited a consistent frontocentral scalp distribution, in agreement with prior studies linking this component to medial frontal control networks (San Martín, 2012; Shahnazian et al., 2018). The present study did not aim to perform precise neuroanatomical localization, and inferences regarding neural generators should be interpreted as indirect and model-based, given the spatial limitations of scalp EEG. Nevertheless, the observed temporal dynamics, feedback sensitivity, and topographic consistency of the FRN align with the established role of the medial prefrontal cortex (mPFC), particularly the ACC, in performance monitoring and adaptive control (San Martín, 2012; McLoughlin et al., 2022).
These findings converge with neurophysiological evidence from non-human primates. Sarafyazd and Jazayeri demonstrated that neurons in the mPFC, especially within the ACC, integrate low-level decision confidence and accumulated negative feedback to trigger high-level strategy switches once a threshold is reached. Although our EEG data cannot localize activity to the ACC with certainty, the correspondence between the computational variables reflected in human FRN dynamics and those encoded by primate ACC neurons suggests a shared functional architecture underlying hierarchical decision-making across species.
Rather than providing direct evidence for ACC involvement, we propose that the FRN serves as a temporally precise electrophysiological signature of hierarchical evidence integration processes known, from invasive recordings, to engage medial frontal circuits including the ACC (Shahnazian et al., 2018; Sarafyazd & Jazayeri, 2019). This interpretation is further supported by human neuroimaging and source-localization studies implicating the ACC in feedback processing and adaptive decision-making (Gluth et al., 2014; Pezzetta et al., 2022), while remaining appropriately constrained by the limitations of EEG.
In summary, this study advances our understanding of hierarchical decision-making by demonstrating that FRN dynamics track the integration of feedback history, decision certainty, and urgency within a unified task. By linking human electrophysiological signals with computational and neurophysiological findings from primates, our results position the FRN as a cross-species neural marker of adaptive strategy updating under uncertainty. Future studies combining hierarchical decision-making paradigms with source-localized EEG, fMRI, or intracranial recordings will be essential to directly test the specific contributions of ACC and related medial frontal networks in humans.
Conclusion
In conclusion, the present study demonstrates that the FRN reflects more than a simple evaluation of feedback valence, serving instead as a neural signature of hierarchical evidence integration during adaptive decision-making. Across a unified task, FRN amplitude systematically tracked the accumulation of negative feedback, sensitivity to low-level decision certainty, and rising decision urgency preceding strategic shifts. Critically, FRN enhancement reliably preceded high-level strategy changes, indicating that this signal captures latent evaluative processes that unfold before overt behavioral adaptation.
These findings position the FRN as a temporally precise marker of hierarchical decision dynamics, linking sensory confidence, feedback history, and urgency into a single neural measure. While scalp EEG does not allow for definitive source localization, the observed frontocentral topography and functional connectivity patterns are consistent with the involvement of medial frontal control networks, including regions, such as the anterior cingulate cortex, which have been previously implicated in adaptive control and hierarchical reasoning.
By bridging human electrophysiological evidence with computational and neurophysiological findings from non-human primates, this work supports the view that hierarchical decision-making relies on conserved neural mechanisms across species. Future studies combining hierarchical paradigms with source-localized EEG, fMRI, intracranial recordings, and computational modeling will be essential for directly characterizing the specific neural circuits underlying these adaptive processes and for refining mechanistic accounts of strategy updating under uncertainty.
Ethical Considerations
Compliance with ethical guidelines
This study was approved by the Research Ethics Committees of Iran University of Medical Sciences, Tehran, Iran (Code: IR.IUMS.REC.1399.1081).
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The authors used the laboratory facilities of Shahid Rajaee Teacher Training University and Sharif University of Technology for conducting the experiments.
Authors' contributions
Conceptualization, study design and final approval: all authors; Experiments, data analysis, and writing the original draft: Leyla Yahyaie; Supervision, data interpretation, review and editing: Reza Ebrahimpour.
Conflict of interest
The authors declared no conflict of interest.
Acknowledgments
The authors are grateful to Jamal Esmaily Sadrabadi for his helpful discussions.
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