Personalized neural responses to self and filial reward: Functional and structural responses to motivational cues

Siti Mariam Roslan; Siti Hajar Zabri; Nur Ayunie Ayob; Aini Ismafairus Abd Hamid; Nur Hartini Mohd Taib; Rahimah Zakaria; Sofina Tamam; Hazim Omar; Alwani Liyana Ahmad; Wan Mohd Zahiruddin Wan Mohammad; Aleya Aziz Marzuki; Asma Hayati Ahmad; Siti Mariam Roslan; Siti Hajar Zabri; Nur Ayunie Ayob; Aini Ismafairus Abd Hamid; Nur Hartini Mohd Taib; Rahimah Zakaria; Sofina Tamam; Hazim Omar; Alwani Liyana Ahmad; Wan Mohd Zahiruddin Wan Mohammad; Aleya Aziz Marzuki; Asma Hayati Ahmad

doi:10.3934/Neuroscience.2025029

AIMS Neuroscience

2025, Volume 12, Issue 4: 592-613. doi: 10.3934/Neuroscience.2025029

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Research article

Personalized neural responses to self and filial reward: Functional and structural responses to motivational cues

1.
School of Medical Sciences, Health Campus, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan, Malaysia
2.
Brain & Behaviour Cluster, School of Medical Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan, Malaysia
3.
Faculty of Science and Technology, Universiti Sains Islam Malaysia, 71800 Nilai, Negeri Sembilan, Malaysia
4.
Department for Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany

Received: 08 July 2025 Revised: 24 October 2025 Accepted: 04 November 2025 Published: 19 November 2025

Understanding how individuals interact with reward-related cues in their environment provides insight into the neural mechanisms underlying motivation and personalized behavior. While monetary rewards for self are well studied, the neural basis of socially relevant rewards—such as filial reward—remains less understood. This study investigated functional and structural brain responses to reward gained from a cognitive task performance for self or for parents (filial) using functional MRI (fMRI) and diffusion MRI (dMRI) in young adults, reflecting personalized interaction with environmental cues. Thirty-two healthy young adults (17 males, mean age = 23 ± 1 years) performed a 2-back working memory task cued for reward conditions for self and for parents during fMRI scanning, followed by dMRI acquisition. Participants were categorized based on the reward condition in which they showed the highest score in task performance. Self-reported reward responsiveness scores were also collected. Random-effects fMRI analysis revealed activation of the putamen in the self-reward condition, more than in the filial reward condition. Using this region as a seed, probabilistic tractography was conducted to compute connection probability indices (CPI) to key target areas: anterior cingulate cortex (ACC), posterior cingulate cortex (PCC), dorsolateral and ventrolateral prefrontal cortices, anterior/posterior insula, and amygdala. The nucleus accumbens (NAcc) was included as a comparative seed. While the cue for self-reward elicited activation in the reward area putamen, with higher white matter connectivity from the right putamen to the ACC, a cue for filial reward significantly activated the right insula. Lateralization to the right insula was also seen in the structural connectivity to NAcc in the filial group. Filial reward also displayed a positive relationship between white matter connectivity of left NAcc to PCC with reward responsiveness. These results demonstrate individualized neural responses shaped by the self and social relevance of the reward.
- reward,
- cues,
- filial,
- fMRI,
- dMRI
Citation: Siti Mariam Roslan, Siti Hajar Zabri, Nur Ayunie Ayob, Aini Ismafairus Abd Hamid, Nur Hartini Mohd Taib, Rahimah Zakaria, Sofina Tamam, Hazim Omar, Alwani Liyana Ahmad, Wan Mohd Zahiruddin Wan Mohammad, Aleya Aziz Marzuki, Asma Hayati Ahmad. Personalized neural responses to self and filial reward: Functional and structural responses to motivational cues[J]. AIMS Neuroscience, 2025, 12(4): 592-613. doi: 10.3934/Neuroscience.2025029

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Abstract

Understanding how individuals interact with reward-related cues in their environment provides insight into the neural mechanisms underlying motivation and personalized behavior. While monetary rewards for self are well studied, the neural basis of socially relevant rewards—such as filial reward—remains less understood. This study investigated functional and structural brain responses to reward gained from a cognitive task performance for self or for parents (filial) using functional MRI (fMRI) and diffusion MRI (dMRI) in young adults, reflecting personalized interaction with environmental cues. Thirty-two healthy young adults (17 males, mean age = 23 ± 1 years) performed a 2-back working memory task cued for reward conditions for self and for parents during fMRI scanning, followed by dMRI acquisition. Participants were categorized based on the reward condition in which they showed the highest score in task performance. Self-reported reward responsiveness scores were also collected. Random-effects fMRI analysis revealed activation of the putamen in the self-reward condition, more than in the filial reward condition. Using this region as a seed, probabilistic tractography was conducted to compute connection probability indices (CPI) to key target areas: anterior cingulate cortex (ACC), posterior cingulate cortex (PCC), dorsolateral and ventrolateral prefrontal cortices, anterior/posterior insula, and amygdala. The nucleus accumbens (NAcc) was included as a comparative seed. While the cue for self-reward elicited activation in the reward area putamen, with higher white matter connectivity from the right putamen to the ACC, a cue for filial reward significantly activated the right insula. Lateralization to the right insula was also seen in the structural connectivity to NAcc in the filial group. Filial reward also displayed a positive relationship between white matter connectivity of left NAcc to PCC with reward responsiveness. These results demonstrate individualized neural responses shaped by the self and social relevance of the reward.

Acknowledgments

This research was funded by the Ministry of Higher Education (MOHE) Malaysia, grant number FRGS/1/2019/SKK03/USM/02/4. We extend our gratitude to the MRI technologists, Wan Nazyrah Abdul Halim, Che Munirah Che Abdullah, and Siti Afidah Mamat, for their invaluable assistance with data acquisition.

Conflict of interest

The authors declare no conflict of interest.

Authors' contributions

Conceptualization, AHA, AIAH, NHMT, ST, and AAM; methodology, AHA, AIAH, and HO; software, AIAH, SMR, SHZ, and NAA; validation, NHMT, ST, and AAM; formal analysis, AIAH, SMR, SHZ, NAA, and WMZWM; investigation, SMR, SHZ, NAA, HO, and ALA; writing—original draft preparation, SMR and AHA; writing—review and editing, RZ, AIAH; supervision, AHA and AIAH; funding acquisition, AHA.

References

[1]	UptvThe Other Christmas Gift (2015). [cited 2025 November 18]. Available from: https://www.youtube.com/watch?v=NSH9k99M31Y
[2]	Filkowski MM, Cochran RN, Haas BW (2016) Altruistic behavior: mapping responses in the brain. Neurosci Neuroecon 5: 65-75. https://doi.org/10.2147/NAN.S87718
[3]	Cutler J, Campbell-Meiklejohn D (2019) A comparative fMRI meta-analysis of altruistic and strategic decisions to give. Neuroimage 1: 227-241. https://doi.org/10.1016/j.neuroimage.2018.09.009
[4]	van de Groep S, Sweijen SW, de Water E, et al. (2023) Temporal discounting for self and friends in adolescence: A fMRI study. Dev Cogn Neurosci 60: 101204. https://doi.org/10.1016/j.dcn.2023.101204
[5]	Zhou Y, Han S, Kang P, et al. (2024) The social transmission of empathy relies on observational reinforcement learning. Proc Natl Acad Sci U S A 121: e2313073121. https://doi.org/10.1073/pnas.2313073121
[6]	Marsh AA, Stoycos SA, Brethel-Haurwitz KM, et al. (2014) Neural and cognitive characteristics of extraordinary altruists. Proc Natl Acad Sci U S A 111: 15036-15041. https://doi.org/10.1073/pnas.1408440111
[7]	Wu Y, Mai N, Weng X, et al. (2020) Changes of Altruistic Behavior and Kynurenine Pathway in Late-Life Depression. Front Psychiatry 11: 338. https://doi.org/10.3389/fpsyt.2020.00338
[8]	Yang Z, Li P (2025) Decoding the altruistic brain: An ALE meta-analysis of the functional localization of giving behaviors. Neurosci Biobehav Rev 174: 106205. https://doi.org/10.1016/j.neubiorev.2025.106205
[9]	Banich MT, Floresco S (2019) Reward systems, cognition, and emotion: Introduction to the special issue. Cogn Affect Behav Neurosci 19: 409-414. https://doi.org/10.3758/s13415-019-00725-z
[10]	Park HR, Verhelst H, Quak M, et al. (2021) Associations between different white matter properties and reward-based performance modulation. Brain Struct Funct 226: 1007-1021. https://doi.org/10.1007/s00429-021-02222-x
[11]	Solomonov N, Victoria LW, Lyons K, et al. (2023) Social reward processing in depressed and healthy individuals across the lifespan: A systematic review and a preliminary coordinate-based meta-analysis of fMRI studies. Behav Brain Res 454: 114632. https://doi.org/10.1016/j.bbr.2023.114632
[12]	Ahmad AH, Zabri SH, Roslan SM, et al. (2024) Diffusion Magnetic Resonance Imaging and Human Reward System Research: A Bibliometric Analysis and Visualisation of Current Research Trends. Malays J Med Sci 31: 111-125. https://doi.org/10.21315/mjms2024.31.4.9
[13]	Mallahzadeh A, Shafie M, Tahvilian M, et al. (2023) White matter tracts alterations underpinning reward and conflict processing. J Affect Disord 331: 251-258. https://doi.org/10.1016/j.jad.2023.03.070
[14]	Glover GH (2011) Overview of functional magnetic resonance imaging. Neurosurg Clin N Am 22: 133-139, vii. https://doi.org/10.1016/j.nec.2010.11.001
[15]	Hagmann P, Jonasson L, Maeder P, et al. (2006) Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics 26 Suppl 1: S205-223. https://doi.org/10.1148/rg.26si065510
[16]	Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35: 4-26. https://doi.org/10.1038/npp.2009.129
[17]	Delgado MR (2007) Reward-related responses in the human striatum. Ann N Y Acad Sci 1104: 70-88. https://doi.org/10.1196/annals.1390.002
[18]	Chantranupong L, Beron CC, Zimmer JA, et al. (2023) Dopamine and glutamate regulate striatal acetylcholine in decision-making. Nature 621: 577-585. https://doi.org/10.1038/s41586-023-06492-9
[19]	Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60: 543-554. https://doi.org/10.1016/j.neuron.2008.11.005
[20]	Ena S, de Kerchove d'Exaerde A, Schiffmann SN (2011) Unraveling the differential functions and regulation of striatal neuron sub-populations in motor control, reward, and motivational processes. Front Behav Neurosci 5: 47. https://doi.org/10.3389/fnbeh.2011.00047
[21]	Gujar N, Yoo SS, Hu P, et al. (2011) Sleep deprivation amplifies reactivity of brain reward nnetworks, biasing the appraisal of positive emotional experiences. J Neurosci 31: 4466-4474. https://doi.org/10.1523/JNEUROSCI.3220-10.2011
[22]	Oldham S, Murawski C, Fornito A, et al. (2018) The anticipation and outcome phases of reward and loss processing: A neuroimaging meta-analysis of the monetary incentive delay task. Hum Brain Mapp 39: 3398-3418. https://doi.org/10.1002/hbm.24184
[23]	Leh SE, Ptito A, Chakravarty MM, et al. (2007) Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neurosci Lett 419: 113-118. https://doi.org/10.1016/j.neulet.2007.04.049
[24]	Jarbo K, Verstynen TD (2015) Converging structural and functional connectivity of orbitofrontal, dorsolateral prefrontal, and posterior parietal cortex in the human striatum. J Neurosci 35: 3865-3878. https://doi.org/10.1523/JNEUROSCI.2636-14.2015
[25]	Cauda F, Cavanna AE, D'agata F, et al. (2011) Functional Connectivity and Coactivation of the Nucleus Accumbens: A Combined Functional Connectivity and Structure-Based Meta-analysis. J Cogn Neurosci 23: 2864-2877. https://doi.org/10.1162/jocn.2011.21624
[26]	Yaple ZA, Yu R, Arsalidou M (2020) Spatial migration of human reward processing with functional development: Evidence from quantitative meta-analyses. Hum Brain Mapp 41: 3993-4009. https://doi.org/10.1002/hbm.25103
[27]	Chaplin TM, Mauro KL, Niehaus CE (2022) Effects of Parenting Environment on Child and Adolescent Social-Emotional Brain Function. Curr Top Behav Neurosci 54: 341-372. https://doi.org/10.1007/7854_2021_276
[28]	Casement MD, Guyer AE, Hipwell AE, et al. (2014) Girls' challenging social experiences in early adolescence predict neural response to rewards and depressive symptoms. Dev Cogn Neurosci 8: 18. https://doi.org/10.1016/j.dcn.2013.12.003
[29]	Guerra P, Campagnoli RR, Vico C, et al. (2011) Filial versus romantic love: contributions from peripheral and central electrophysiology. Biol Psychol 88: 196-203. https://doi.org/10.1016/j.biopsycho.2011.08.002
[30]	Buckner RL, DiNicola LM (2019) The brain's default network: updated anatomy, physiology and evolving insights. Nat Rev Neurosci 20: 593-608. https://doi.org/10.1038/s41583-019-0212-7
[31]	Fey MV, Naufel K, Locker L (2016) Working memory and cued recall. Honors College Theses . [cited 2025 November 04]. Available from: https://digitalcommons.georgiasouthern.edu/honors-theses/220
[32]	Vila J, Morato C, Lucas I, et al. (2019) The affective processing of loved familiar faces and names: Integrating fMRI and heart rate. PLoS One 14: e0216057. https://doi.org/10.1371/journal.pone.0216057
[33]	Tamam S, Ahmad AH, Kamil WA (2018) Modelling brain activations and connectivity of pain modulated by having a loved one nearby. AIP Conf Proc 1972: 030008. https://doi.org/10.1063/1.5041229
[34]	Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-113. https://doi.org/10.1016/0028-3932(71)90067-4
[35]	Van den Berg I, Franken IH, Muris P (2010) A new scale for measuring reward responsiveness. Front Psychol 1: 239. https://doi.org/10.3389/fpsyg.2010.00239
[36]	Esteban O, Markiewicz CJ, Blair RW, et al. (2019) fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat Methods 16: 111-116. https://doi.org/10.1038/s41592-018-0235-4
[37]	Sumardi NBB, Ying JH, Hamid AIA (2022) A preliminary fMRI study of relative clause in comprehension among native and non-native Malay language speakers. Neurosci Res Note 5: 113. https://doi.org/10.31117/neuroscirn.v5i1.113
[38]	Ashburner J, Barnes G, Chen CC, et al. SPM12 Manual the FIL Methods Group (and honorary members) (2021). [cited 2025 November 04]. Available from: https://www.fil.ion.ucl.ac.uk/spm/
[39]	Di X, Biswal BB (2023) A functional MRI pre-processing and quality control protocol based on statistical parametric mapping (SPM) and MATLAB. Front Neuroimaging 1: 1070151. https://doi.org/10.3389/fnimg.2022.1070151
[40]	Strappini F, Gilboa E, Pitzalis S, et al. (2017) Adaptive smoothing based on Gaussian processes regression increases the sensitivity and specificity of fMRI data. Hum Brain Mapp 38: 1438-1459. https://doi.org/10.1002/hbm.23464
[41]	Holmes AP, Friston KJ (1998) Generalisability, Random Effects & Population Inference. Neuroimage 7: S754. https://doi.org/10.1016/S1053-8119(18)31587-8
[42]	Behrens TEJ, Woolrich MW, Jenkinson M, et al. (2003) Characterization and Propagation of Uncertainty in Diffusion-Weighted MR Imaging. Magn Reson Med 50: 1077-1088. https://doi.org/10.1002/mrm.10609
[43]	Smith SM, Jenkinson M, Woolrich MW, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1: S208-19. https://doi.org/10.1016/j.neuroimage.2004.07.051
[44]	Smith SM (2002) Fast robust automated brain extraction (2002). Hum Brain Mapp 17: 143-155. https://doi.org/10.1002/hbm.10062
[45]	Camara E, Rodriguez-fornells A, Ye Z, et al. (2009) Reward networks in the brain as captured by connectivity measures. Front Neurosci 3: 350-362. https://doi.org/10.3389/neuro.01.034.2009
[46]	Zabri SH, Ahmad AH, Zakaria R, et al. (2023) Probabilistic Tractography Between Nucleus Accumbens and Other Reward-related Brain Areas in Malay Female Adolescents. Mal J Med Health Sci 19: 61-68. https://doi:10.47836/mjmhs19.2.11
[47]	Wang W, Yan X, He X, et al. (2024) Evidence for the Beneficial Effect of Reward on Working Memory: A Meta-Analytic Study. J Intell 12: 88. https://doi.org/10.3390/jintelligence12090088
[48]	Oren S, Tittgemeyer M, Rigoux L, et al. (2022) Neural encoding of food and monetary reward delivery. Neuroimage 257: 119335. https://doi.org/10.1016/j.neuroimage.2022.119335
[49]	Hill KE, Dickey L, Pegg S, et al. (2023) Associations between parental conflict and social and monetary reward responsiveness in adolescents with clinical depression. Res Child Adolesc Psychopathol 51: 119-131. https://doi.org/10.1007/s10802-022-00949-7
[50]	Wang D, Liu T, Shi J (2020) Neural Dynamic Responses of Monetary and Social Reward Processes in Adolescents. Front Hum Neurosci 14: 141. https://doi.org/10.3389/fnhum.2020.00141
[51]	Delgado MR, Fareri DS, Chang LJ (2023) Characterizing the mechanisms of social connection. Neuron 111: 3911-3925. https://doi.org/10.1016/j.neuron.2023.09.012
[52]	Punjvani MB (2015) Effect of parenting styles and family income on altruism in adolescents. Int J Indian Psychol 5: 126-140. https://doi.org/10.25215/0203.057
[53]	Chan YC, Hsu WC, Chou TL (2018) Dissociation between the processing of humorous and monetary rewards in the ‘motivation’ and ‘hedonic’ brains. Sci Rep 8: 15425. https://doi.org/10.1038/s41598-018-33623-4
[54]	Chan YC, Wang CY, Chou TL (2023) Money or funny: Effective connectivity during service recovery with a DCM-PEB approach. Biol Psychol 176: 108464. https://doi.org/10.1016/j.biopsycho.2022.108464
[55]	Jauhar S, Fortea L, Solanes A, et al. (2021) Brain activations associated with anticipation and delivery of monetary reward: A systematic review and meta-analysis of fMRI studies. PLoS One 16: e0255292. https://doi.org/10.1371/journal.pone.0255292
[56]	Cao Z, Bennett M, Orr C, et al. (2019) Mapping adolescent reward anticipation, receipt, and prediction error during the monetary incentive delay task. Hum Brain Mapp 40: 262-283. https://doi.org/10.1002/hbm.24370
[57]	Delgado MR, Nystrom LE, Fissell C, et al. (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84: 3072-3077. https://doi.org/10.1152/jn.2000.84.6.3072
[58]	Ren P, Hou G, Ma M, et al. (2023) Enhanced putamen functional connectivity underlies altered risky decision-making in age-related cognitive decline. Sci Rep 13: 6619. https://doi.org/10.1038/s41598-023-33634-w
[59]	Salehinejad MA, Ghanavati E, Rashid MHA, et al. (2021) Hot and cold executive functions in the brain: A prefrontal-cingular network. Brain Neurosci Adv 5: 239821282110077. https://doi.org/10.1177/23982128211007769
[60]	Schröter N, Rijntjes M, Urbach H, et al. (2022) Disentangling nigral and putaminal contribution to motor impairment and levodopa response in Parkinson's disease. NPJ Parkinsons Dis 8: 132. https://doi.org/10.1038/s41531-022-00401-z
[61]	Shen B, Pan Y, Jiang X, et al. (2020) Altered putamen and cerebellum connectivity among different subtypes of Parkinson's disease. CNS Neurosci Ther 26: 207-214. https://doi.org/10.1111/cns.13259
[62]	Brewer JA, Garrison KA, Whitfield-Gabrieli S (2013) What about the “Self” is Processed in the Posterior Cingulate Cortex?. Front Hum Neurosci 7: 647. https://doi.org/10.3389/fnhum.2013.00647
[63]	Li X, Pan Y, Fang Z, et al. (2020) Test-retest reliability of brain responses to risk-taking during the balloon analogue risk task. Neuroimage 209: 116495. https://doi.org/10.1016/j.neuroimage.2019.116495
[64]	Hu W, Zhao X, Liu Y, et al. (2022) Reward sensitivity modulates the brain reward pathway in stress resilience via the inherent neuroendocrine system. Neurobiol Stress 20: 100485. https://doi.org/10.1016/j.ynstr.2022.100485
[65]	Soutschek A, Tobler PN (2020) Causal role of lateral prefrontal cortex in mental effort and fatigue. Hum Brain Mapp 41: 4630-4640. https://doi.org/10.1002/hbm.25146
[66]	Barch DM, Pagliaccio D, Luking K (2016) Mechanisms underlying motivational deficits in psychopathology: Similarities and differences in depression and schizophrenia. Curr Top Behav Neurosci 27: 411-449. https://doi.org/10.1007/7854_2015_376
[67]	Miró-Padilla A, Adrián-Ventura J, Cherednichenko A, et al. (2023) Relevance of the anterior cingulate cortex volume and personality in motivated physical activity behaviors. Commun Biol 6: 1106. https://doi.org/10.1038/s42003-023-05423-8
[68]	Craig AD (2009) How do you feel--now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70. https://doi.org/10.1038/nrn2555
[69]	Namkung H, Kim SH, Sawa A (2017) The Insula: An Underestimated Brain Area in Clinical Neuroscience, Psychiatry, and Neurology. Trends Neurosci 40: 200-207. https://doi.org/10.1016/j.tins.2017.02.002
[70]	Koch K, Wagner G, Schachtzabel C, et al. (2014) Association between white matter fiber structure and reward-related reactivity of the ventral striatum. Hum Brain Mapp 35: 1469-1476. https://doi.org/10.1002/hbm.22284
[71]	Xu J, Kober H, Carroll KM, et al. (2012) White matter integrity and behavioral activation in healthy subjects. Hum Brain Mapp 33: 994-1002. https://doi.org/10.1002/hbm.21275

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