The development of aperiodic neural activity in the human brain - PubMed (original) (raw)

. 2025 Dec;9(12):2548-2563.

doi: 10.1038/s41562-025-02270-x. Epub 2025 Jul 15.

Samantha M Gray 2 3, Adam J O Dede 2, Yessenia M Rivera 2, Qin Yin 4 5, Parisa Vahidi 4, Elias M B Rau 6, Christopher Cyr 2, Ania M Holubecki 2, Eishi Asano 4, Jack J Lin 7, Olivia Kim McManus 8, Shifteh Sattar 8, Ignacio Saez 7 9, Fady Girgis 7 10, David King-Stephens 11 12, Peter B Weber 11, Kenneth D Laxer 11, Stephan U Schuele 2, Joshua M Rosenow 2, Joyce Y Wu 2 13, Sandi K Lam 2 13, Jeffrey S Raskin 2 13, Edward F Chang 14, Ammar Shaikhouni 15, Peter Brunner 16, Jarod L Roland 16 17, Rodrigo M Braga 2, Robert T Knight 18, Noa Ofen 4 5, Elizabeth L Johnson 2

Affiliations

The development of aperiodic neural activity in the human brain

Zachariah R Cross et al. Nat Hum Behav. 2025 Dec.

Abstract

The neurophysiological mechanisms supporting brain maturation are fundamental to attention and memory capacity across the lifespan. Human brain regions develop at different rates, with many regions developing into the third and fourth decades of life. Here, in this preregistered study ( https://osf.io/gsru7 ), we analysed intracranial electroencephalography recordings from widespread brain regions in a large developmental cohort. Using task-based (that is, attention to to-be-remembered visual stimuli) and task-free (resting-state) data from 101 children and adults (5.93-54.00 years, 63 males; n electrodes = 5,691), we mapped aperiodic (1/ƒ-like) activity, a proxy of neural noise, where steeper slopes indicate less noise and flatter slopes indicate more noise. We reveal that aperiodic slopes flatten with age into young adulthood in both association and sensorimotor cortices, challenging models of early sensorimotor development based on brain structure. In the prefrontal cortex (PFC), attentional state modulated age effects, revealing steeper task-based than task-free slopes in adults and the opposite in children, consistent with the development of cognitive control. Age-related differences in task-based slopes also explained age-related gains in memory performance, linking the development of PFC cognitive control to the development of memory. Last, with additional structural imaging measures, we reveal that age-related differences in grey matter volume are similarly associated with aperiodic slopes in association and sensorimotor cortices. Our findings establish developmental trajectories of aperiodic activity in localized brain regions and illuminate the development of PFC control during adolescence in the development of attention and memory.

© 2025. The Author(s), under exclusive licence to Springer Nature Limited.

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Conflict of interest statement

Competing interests: The authors declare no competing interests.

Figures

Figure 1.

Figure 1.. Design, channel coverage, and key variables.

(A) Intracranial neurophysiological activity was recorded using electrocorticography (ECoG; middle) and stereoelectroencephalography (sEEG; bottom) during both task-based (top left) and task-free wake states (top right). (B) Seizure- and artifact-free intracranial channel placements (n = 5691) across all patients (n = 101) in MNI space. (C) Schematic of key dependent and independent variables. Top left: iEEG patients (teal; n = 81) show the expected developmental trajectory of improved memory recognition from ~5 – 30 years of age (one-sided non-linear regression, p <0.001) and fall in the range of age-matched, healthy controls (gray; n = 221). Shading indicates 83% CIs. Top right: schematic power spectral density plot illustrating the periodic (oscillatory) components over and above the aperiodic (1/ƒ-like) component in task-free (dashed) and task-based (solid) conditions. The offset (i.e., y-intercept) and slope (exponent) make up the aperiodic component when power (y-axis) is in log-space. Bottom left: TI MRI obtained for each patient, parcellation of cortical regions based on the Desikan-Killiany-Tourville atlas, and GMV estimation (adapted from). Bottom right: age-related differences in global GMV (mm3) in our cohort, showing the expected developmental trajectory of decreased GMV from ~5 – 54 years of age (one-sided linear regression, p <0.001).

Figure 2.

Figure 2.. Regional differences in the aperiodic slope and correlations with GMV.

(A) Brain-wide standardized means (predicted marginal means) of regional aperiodic slopes adjusted across attentional state, age and the random effects structures. Warmer colors/higher values indicate steeper slopes. (B) Brain-wide correlations (one-sided, FDR-corrected Spearman correlations) between regional GMV (mm3) and aperiodic slopes. Warmer colors/higher values indicate positive correlations; cooler colors/lower values indicate negative correlations. Note that the area corresponding to subcortical space is white as no analysis of subcortical GMV was performed. Regions with statistically significant correlations (p < 0.05) are indicated by dashed borders. (C) Scatterplots illustrating relationships between GMV (x-axis) and aperiodic slopes in regions with statistically significant correlations. Individual data points represent single participant data averaged across channels for each representative ROI. Shading shows the standard error. (D) Ridgeline plot illustrating the distribution of aperiodic slopes (x-axis; higher values denote a steeper slope) by region (y-axis) and condition (left: task-free; right: task-based).

Figure 3.

Figure 3.. Age-related differences in aperiodic slopes between association and sensorimotor cortices.

Modelled effects for differences in the aperiodic slope (y-axis; higher values denote a steeper slope) by age (x-axis). Association cortices are presented in teal and sensorimotor cortices in orange. Shading indicates 83% CIs. Individual data points represent slope values per participant averaged over channels.

Figure 4.

Figure 4.. Regions with a significant interaction between age and attentional state on aperiodic activity.

(A) Brain-wide age and condition interactions on regional aperiodic slopes. Regions with statistically significant interactions between age and attentional state (FDR < 0.05) are indicated by dashed borders. (B) Scatterplots illustrating interactions between age (x-axis; in years) and attentional state (red = task-based; gray = task-free) on the aperiodic slope (y-axis; higher values denote a steeper slope) in regions with statistically significant interactions. Individual data points represent single participant data averaged across channels for each representative ROI. Shading indicates 83% CIs.

Figure 5.

Figure 5.. Task-based aperiodic slopes in MFG predict age-related differences in memory performance.

(A) Brain-wide slope and age interactions on memory (one-sided, FDR-corrected linear regressions), with rMFG demonstrating statistically significant interactions between the task-based slopes and age (p <0.05) on memory performance, with this indicated by dashed borders. (B) Scatterplot illustrating interactions between task-based rMFG slopes (y-axis; higher values denote a steeper slope) and age (x-axis; in years) on memory (z-scale; warmer colors denote higher memory recognition accuracy). Individual data points represent single participant data averaged across channels for each representative ROI. Shading shows the standard error.

Figure 6.

Figure 6.. Regions with a significant effect of age on GMV.

(A) Brain-wide correlations (one-sided Pearson r correlations) between regional GMV (mm3) and age (in years). Warmer colors/higher values indicate positive correlations and cooler colors/lower values indicate negative correlations. Note that the area corresponding to subcortical space is white as no analysis of subcortical GMV was performed. Regions with statistically significant correlations (p < 0.05) are indicated by dashed borders. (B) Scatterplots illustrating relationships between GMV (y-axis) and age (x-axis) in regions with statistically significant correlations. Shaded areas indicate the standard error of the mean.

Figure 7.

Figure 7.. Regions with a significant interaction between age and GMV on the aperiodic slope.

(A) Top row: Brain-wide GMV and age interactions on regional aperiodic slopes. Regions with statistically significant interactions between age and GMV (FDR < 0.05) are indicated by dashed borders. Bottom row: scatterplots illustrating interactions between age (x-axis; in years) and GMV (z-scale; warmer colors denote higher GMV) on the aperiodic slopes (y-axis; higher values denote a steeper slope) in regions with statistically significant interactions. Individual data points represent single participant data averaged across channels for each representative ROI. Shading shows the standard error.

Figure 8.

Figure 8.. Aperiodic activity stabilizes in young adulthood, differs by age and attentional state, predicts age-related variability in episodic memory, and is associated with age-related variability in GMV.

(A) Aperiodic slopes in sensorimotor (orange) and association (teal) cortices flatten from age 5 – 25 years and steepen thereafter. Note that the flattening is more pronounced in sensorimotor than association cortices in adolescence and young adulthood (gray shading). Regarding attentional state (i.e., task-based vs. task-free) differences in aperiodic activity, in PFC, task-free (dashed red) slopes are steeper (i.e., less neural noise) than task-based (solid red) slopes in children, and the inverse is observed in adults. Effects reverse at ~18 – 20 years of age, likely reflecting the development of control. Shading indicates 83% CIs. (B) PFC-derived aperiodic slopes during task-based but not task-free states predicted age-related variability in memory performance, whereby the age-related flattening of aperiodic slopes was associated with age-related improvements in memory. Flatter sensorimotor cortical slopes were not associated with better memory performance after accounting for age. (C) Modeling the relationship between brain volume and aperiodic slopes revealed similar age-related differences in structure-function coupling. In both posterior cingulate cortex and postcentral gyrus, slopes were steeper in childhood regardless of GMV; in adolescence and adulthood, lower GMV was associated with steeper slopes and higher GMV was associated with flatter slopes. Shading indicates 83% CIs.

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