Heritability of Moment-to-Moment Neural Variability During Emotion Recognition

871 

Abstract Submission 

Tugce Yildiz-Ahola¹, Fredrik Åhs², Jörgen Rosén^1,2, Granit Kastrati¹, Tomas Furmark³, Douglas Garrett^4,5, Kristoffer Månsson^1,6

¹Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden, ²Department of Psychology and Social Work, Mid Sweden University, Östersund, Sweden, ³Department of Psychology, Emotion Psychology, Uppsala University, Uppsala, Sweden, ⁴Center for Lifespan Psychology, Max Plank Institute for Human Development, Berlin, Germany, ⁵Max Planck, UCL Centre for Computational Psychiatry and Ageing Research, Berlin, Germany, ⁶Department of Clinical Psychology and Psychotherapy, Babeș-Bolyai University, Cluj-Napoca, Romania

Tugce Yildiz-Ahola  
Department of Clinical Neuroscience, Karolinska Institutet
Stockholm, Sweden

Fredrik Åhs  
Department of Psychology and Social Work, Mid Sweden University
Östersund, Sweden

Jörgen Rosén  
Department of Clinical Neuroscience, Karolinska Institutet|Department of Psychology and Social Work, Mid Sweden University
Stockholm, Sweden|Östersund, Sweden

Granit Kastrati  
Department of Clinical Neuroscience, Karolinska Institutet
Stockholm, Sweden

Tomas Furmark  
Department of Psychology, Emotion Psychology, Uppsala University
Uppsala, Sweden

Douglas Garrett  
Center for Lifespan Psychology, Max Plank Institute for Human Development|Max Planck, UCL Centre for Computational Psychiatry and Ageing Research
Berlin, Germany|Berlin, Germany

Kristoffer Månsson  
Department of Clinical Neuroscience, Karolinska Institutet|Department of Clinical Psychology and Psychotherapy, Babeș-Bolyai University
Stockholm, Sweden|Cluj-Napoca, Romania

Heritability, the extent to which differences in traits can be attributed to genetic factors, plays a fundamental role in shaping brain function. In functional magnetic resonance imaging (fMRI), the average blood-oxygen-level-dependent (BOLD) signal across time/trials (i.e., MEANBOLD remains the typical approach in task-based fMRI studies. This model disregards variability from trial to trial as unwanted noise. In contrast, a growing body of evidence has shown that moment-to-moment variability in the BOLD signal (e.g., standard deviation of the BOLD response; SDBOLD) represents a viable measure of brain function. For instance, neural variability to socio-emotional faces has shown both high test-retest reliability, and sensitivity to inter-individual differences (Månsson et al. 2022). Further, identifying facial emotions is an inherent human skill and crucial for social interactions. Even though the ability to recognize emotions in faces is facilitated by a fundamental neural circuit (Haxby, Hoffman, and Gobbini 2002), the genetic contribution to this ability is overlooked. Therefore, this study explores genetic influence on socio-emotional moment-to-moment neural variability during emotion recognition while going beyond traditional measures.

To investigate the heritability of BOLD-fMRI signals during an emotion recognition task, we employed a classical twin design with 144 pairs (69 monozygotic (MZ) and 75 dizygotic (DZ); N=288). Participants performed an emotion recognition task while scanned with MRI (3T General Electric), consisting of 4 emotional face and 5 geometrical shape matching blocks. The MR scanning parameters were set with a repetition time (TR) of 2.4 seconds, resulting in a total of 160 volumes. The heritability of brain signals was estimated using the fast and non-iterative APACE (Accelerated Permutation Inference for ACE model) method, which calculates the influence of additive genetics (A), shared environment (C), and unique environment (E) on phenotypic variance. Age and sex were included as covariates to control for their potential effects. Heritability (h2) is the measure of the proportion of phenotypic variance that is attributable to additive genetics and is obtained through statistical methods embedded in APACE. Statistical comparisons were performed voxel-wise (whole-brain) in MZ and DZ twin pairs. Significant clusters of heritability were defined with a whole-brain cluster-wise Family-Wise Error (FWE) correction threshold with alpha set at P < 0.05.

The heritability (voxel-wise, averaged h2 across the whole-brain) of emotion recognition neural variability (SDBOLD) was statistically significant (h2 = 0.25, 95% CI 0.12, 0.39; permuted P = 0.029) and more than twice as high relative to the non-significant heritability of MEANBOLD emotion recognition (h2 = 0.10, 95% CI 0.05, 0.16; permuted P = 0.240). FWE corrected, significant clusters of SDBOLD emotion recognition heritability included the occipital lingual gyrus (h2 = 0.69), anterior cingulate cortex (h2= 0.61), parahippocampal gyrus (h2= 0.56), and thalamus (h2 = 0.62).

Our study demonstrates that moment-to-moment neural variability during an emotion recognition task is more heritable than average neural responses, highlighting the importance of variability in brain activity in heritability estimates. Our findings revealed significant clusters of heritability for SDBOLD in specific brain regions implicated in emotional face processing. These include the anterior cingulate gyrus and the parahippocampal gyrus that are activated during emotional face recognition (Xu et al. 2021) (Zhao et al. 2017), and the thalamus with its damage leading to an impairment in facial emotion recognition (Cheung et al. 2006). These identified clusters provide valuable insights into the genetic influences on moment-to-moment variability during the task of emotional face recognition. SDBOLD could be a new and more powerful signature of how genetics influence brain function.

Emotional Perception

Genetics Other ¹

Activation (eg. BOLD task-fMRI) ²

Emotions

FUNCTIONAL MRI

Other - Heritability