Skip to main content
Top
Published in: Brain Structure and Function 6/2023

22-06-2023 | Original Article

Using modular connectome-based predictive modeling to reveal brain-behavior relationships of individual differences in working memory

Authors: Huayi Yang, Junjun Zhang, Zhenlan Jin, Pouya Bashivan, Ling Li

Published in: Brain Structure and Function | Issue 6/2023

Login to get access

Abstract

Working memory plays a crucial role in our daily lives, and brain imaging has been used to predict working memory performance. Here, we present an improved connectome-based predictive modeling approach for building a predictive model of individual working memory performance from whole-brain functional connectivity. The model was built using n-back task-based fMRI and resting-state fMRI data from the Human Connectome Project. Compared to prior models, our model was more interpretable, demonstrated a closer connection to the known anatomical and functional network. The model also demonstrates strong generalization on nine other cognitive behaviors from the HCP database and can well predict the working memory performance of healthy individuals in external datasets. By comparing the differences in prediction effects of different brain networks and anatomical feature analysis on n-back tasks, we found the essential role of some networks in differentiating between high and low working memory loads conditions.
Literature
go back to reference Avery EW, Yoo K, Rosenberg MD, Greene AS, Gao S, Na DL, Scheinost D, Constable TR, Chun MM (2020) Distributed patterns of functional connectivity predict working memory performance in novel healthy and memory-impaired individuals. J Cogn Neurosci 32(2):241–255PubMedCrossRef Avery EW, Yoo K, Rosenberg MD, Greene AS, Gao S, Na DL, Scheinost D, Constable TR, Chun MM (2020) Distributed patterns of functional connectivity predict working memory performance in novel healthy and memory-impaired individuals. J Cogn Neurosci 32(2):241–255PubMedCrossRef
go back to reference Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J (2007) Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 27(29):7807–7816PubMedPubMedCentralCrossRef Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J (2007) Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 27(29):7807–7816PubMedPubMedCentralCrossRef
go back to reference Baddeley A (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4(11):417–423PubMedCrossRef Baddeley A (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4(11):417–423PubMedCrossRef
go back to reference Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4(10):829–839PubMedCrossRef Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4(10):829–839PubMedCrossRef
go back to reference Bauer RH, Fuster JM (1976) Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. J Comp Physiol Psychol 90(3):293PubMedCrossRef Bauer RH, Fuster JM (1976) Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. J Comp Physiol Psychol 90(3):293PubMedCrossRef
go back to reference Cai W, Ryali S, Pasumarthy R, Talasila V, Menon V (2021) Dynamic causal brain circuits during working memory and their functional controllability. Nat Commun 12(1):1–16CrossRef Cai W, Ryali S, Pasumarthy R, Talasila V, Menon V (2021) Dynamic causal brain circuits during working memory and their functional controllability. Nat Commun 12(1):1–16CrossRef
go back to reference Cowan N (2014) Working memory underpins cognitive development, learning, and education. Educ Psychol Rev 26(2):197–223PubMedCrossRef Cowan N (2014) Working memory underpins cognitive development, learning, and education. Educ Psychol Rev 26(2):197–223PubMedCrossRef
go back to reference Delawalla Z, Barch DM, Fisher Eastep JL, Thomason ES, Hanewinkel MJ, Thompson PA, Csernansky JG (2006) Factors mediating cognitive deficits and psychopathology among siblings of individuals with schizophrenia. Schizophr Bull 32(3):525–537PubMedPubMedCentralCrossRef Delawalla Z, Barch DM, Fisher Eastep JL, Thomason ES, Hanewinkel MJ, Thompson PA, Csernansky JG (2006) Factors mediating cognitive deficits and psychopathology among siblings of individuals with schizophrenia. Schizophr Bull 32(3):525–537PubMedPubMedCentralCrossRef
go back to reference Dryburgh E, McKenna S, Rekik I (2020) Predicting full-scale and verbal intelligence scores from functional connectomic data in individuals with autism spectrum disorder. Brain Imaging Behav 14(5):1769–1778PubMedCrossRef Dryburgh E, McKenna S, Rekik I (2020) Predicting full-scale and verbal intelligence scores from functional connectomic data in individuals with autism spectrum disorder. Brain Imaging Behav 14(5):1769–1778PubMedCrossRef
go back to reference Eryilmaz H, Dowling KF, Hughes DE, Rodriguez-Thompson A, Tanner A, Huntington C, Coon WG, Roffman JL (2020) Working memory load-dependent changes in cortical network connectivity estimated by machine learning. Neuroimage 217:116895PubMedCrossRef Eryilmaz H, Dowling KF, Hughes DE, Rodriguez-Thompson A, Tanner A, Huntington C, Coon WG, Roffman JL (2020) Working memory load-dependent changes in cortical network connectivity estimated by machine learning. Neuroimage 217:116895PubMedCrossRef
go back to reference Finn ES, Shen X, Scheinost D, Rosenberg MD, Huang J, Chun MM, Papademetris X, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18(11):1664–1671PubMedPubMedCentralCrossRef Finn ES, Shen X, Scheinost D, Rosenberg MD, Huang J, Chun MM, Papademetris X, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18(11):1664–1671PubMedPubMedCentralCrossRef
go back to reference Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61(2):331–349PubMedCrossRef Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61(2):331–349PubMedCrossRef
go back to reference Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173(3997):652–654PubMedCrossRef Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173(3997):652–654PubMedCrossRef
go back to reference Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR (2013) The minimal preprocessing pipelines for the human connectome project. Neuroimage 80:105–124PubMedCrossRef Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR (2013) The minimal preprocessing pipelines for the human connectome project. Neuroimage 80:105–124PubMedCrossRef
go back to reference Haatveit BC, Sundet K, Hugdahl K, Ueland T, Melle I, Andreassen OA (2010) The validity of d prime as a working memory index: results from the “Bergen n-back task.” J Clin Exp Neuropsychol 32(8):871–880PubMedCrossRef Haatveit BC, Sundet K, Hugdahl K, Ueland T, Melle I, Andreassen OA (2010) The validity of d prime as a working memory index: results from the “Bergen n-back task.” J Clin Exp Neuropsychol 32(8):871–880PubMedCrossRef
go back to reference Jiang R, Calhoun VD, Cui Y, Qi S, Zhuo C, Li J, Jung R, Yang J, Du Y, Jiang T (2020a) Multimodal data revealed different neurobiological correlates of intelligence between males and females. Brain Imaging Behav 14(5):1979–1993PubMedPubMedCentralCrossRef Jiang R, Calhoun VD, Cui Y, Qi S, Zhuo C, Li J, Jung R, Yang J, Du Y, Jiang T (2020a) Multimodal data revealed different neurobiological correlates of intelligence between males and females. Brain Imaging Behav 14(5):1979–1993PubMedPubMedCentralCrossRef
go back to reference Jiang R, Zuo N, Ford JM, Qi S, Zhi D, Zhuo C, Xu Y, Fu Z, Bustillo J, Turner JA (2020b) Task-induced brain connectivity promotes the detection of individual differences in brain-behavior relationships. Neuroimage 207:116370PubMedCrossRef Jiang R, Zuo N, Ford JM, Qi S, Zhi D, Zhuo C, Xu Y, Fu Z, Bustillo J, Turner JA (2020b) Task-induced brain connectivity promotes the detection of individual differences in brain-behavior relationships. Neuroimage 207:116370PubMedCrossRef
go back to reference Kelley TA, Lavie N (2011) Working memory load modulates distractor competition in primary visual cortex. Cereb Cortex 21(3):659–665PubMedCrossRef Kelley TA, Lavie N (2011) Working memory load modulates distractor competition in primary visual cortex. Cereb Cortex 21(3):659–665PubMedCrossRef
go back to reference Kirchner WK (1958) Age differences in short-term retention of rapidly changing information. J Exp Psychol 55(4):352PubMedCrossRef Kirchner WK (1958) Age differences in short-term retention of rapidly changing information. J Exp Psychol 55(4):352PubMedCrossRef
go back to reference Kirschen MP, Chen SA, Schraedley-Desmond P, Desmond JE (2005) Load-and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fmri study. Neuroimage 24(2):462–472PubMedCrossRef Kirschen MP, Chen SA, Schraedley-Desmond P, Desmond JE (2005) Load-and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fmri study. Neuroimage 24(2):462–472PubMedCrossRef
go back to reference Klatzky RL (1975) Human memory: structures and processes. W. H. Freeman, P87 Klatzky RL (1975) Human memory: structures and processes. W. H. Freeman, P87
go back to reference Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29(47):14980–14986PubMedPubMedCentralCrossRef Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29(47):14980–14986PubMedPubMedCentralCrossRef
go back to reference Li G, Chen Y, Le TM, Wang W, Tang X, Li C-SR (2021) Neural correlates of individual variation in two-back working memory and the relationship with fluid intelligence. Sci Rep 11(1):1–13 Li G, Chen Y, Le TM, Wang W, Tang X, Li C-SR (2021) Neural correlates of individual variation in two-back working memory and the relationship with fluid intelligence. Sci Rep 11(1):1–13
go back to reference Lin Q, Yoo K, Shen X, Constable RT, Chun MM (2020) A connectome-based prediction model of long-term memory. bioRxiv Lin Q, Yoo K, Shen X, Constable RT, Chun MM (2020) A connectome-based prediction model of long-term memory. bioRxiv
go back to reference Miller G-G, Pribram E (1960) vol 16. Henry Holt and company, New York Miller G-G, Pribram E (1960) vol 16. Henry Holt and company, New York
go back to reference Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25(1):46–59PubMedPubMedCentralCrossRef Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25(1):46–59PubMedPubMedCentralCrossRef
go back to reference Redick TS, Lindsey DR (2013) Complex span and n-back measures of working memory: A meta-analysis. Psychon Bull Rev 20(6):1102–1113PubMedCrossRef Redick TS, Lindsey DR (2013) Complex span and n-back measures of working memory: A meta-analysis. Psychon Bull Rev 20(6):1102–1113PubMedCrossRef
go back to reference Repovš G, Barch DM (2012) Working memory related brain network connectivity in individuals with schizophrenia and their siblings. Front Hum Neurosci 6:137PubMedPubMedCentralCrossRef Repovš G, Barch DM (2012) Working memory related brain network connectivity in individuals with schizophrenia and their siblings. Front Hum Neurosci 6:137PubMedPubMedCentralCrossRef
go back to reference Repovs G, Csernansky JG, Barch DM (2011) Brain network connectivity in individuals with schizophrenia and their siblings. Biol Psychiat 69(10):967–973PubMedCrossRef Repovs G, Csernansky JG, Barch DM (2011) Brain network connectivity in individuals with schizophrenia and their siblings. Biol Psychiat 69(10):967–973PubMedCrossRef
go back to reference Rinck P (2014) Magnetic resonance: a critical peer-reviewed introduction. Magnetic resonance in medicine. The basic textbook of the European magnetic resonance forum. BoD Germany, p 21 Rinck P (2014) Magnetic resonance: a critical peer-reviewed introduction. Magnetic resonance in medicine. The basic textbook of the European magnetic resonance forum. BoD Germany, p 21
go back to reference Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. Neuroimage 60(1):830–846PubMedCrossRef Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. Neuroimage 60(1):830–846PubMedCrossRef
go back to reference Shen X, Tokoglu F, Papademetris X, Constable RT (2013) Groupwise whole-brain parcellation from resting-state fmri data for network node identification. Neuroimage 82:403–415PubMedCrossRef Shen X, Tokoglu F, Papademetris X, Constable RT (2013) Groupwise whole-brain parcellation from resting-state fmri data for network node identification. Neuroimage 82:403–415PubMedCrossRef
go back to reference Shen X, Finn ES, Scheinost D, Rosenberg MD, Chun MM, Papademetris X, Constable RT (2017) Using connectome-based predictive modeling to predict individual behavior from brain connectivity. Nature Protoc 12(3):506–518CrossRef Shen X, Finn ES, Scheinost D, Rosenberg MD, Chun MM, Papademetris X, Constable RT (2017) Using connectome-based predictive modeling to predict individual behavior from brain connectivity. Nature Protoc 12(3):506–518CrossRef
go back to reference Sui J, Jiang R, Bustillo J, Calhoun V (2020) Neuroimaging-based individualized prediction of cognition and behavior for mental disorders and health: methods and promises. Biol Psychiat 88(11):818–828PubMedCrossRef Sui J, Jiang R, Bustillo J, Calhoun V (2020) Neuroimaging-based individualized prediction of cognition and behavior for mental disorders and health: methods and promises. Biol Psychiat 88(11):818–828PubMedCrossRef
go back to reference Talati A, Hirsch J (2005) Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on what, when, and where related information: an fmri study. J Ccogn Neurosci 17(7):981–993CrossRef Talati A, Hirsch J (2005) Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on what, when, and where related information: an fmri study. J Ccogn Neurosci 17(7):981–993CrossRef
go back to reference Van Essen DC, Ugurbil K, Auerbach E, Barch D, Behrens TE, Bucholz R, Chang A, Chen L, Corbetta M, Curtiss SW (2012) The human connectome project: a data acquisition perspective. Neuroimage 62(4):2222–2231PubMedCrossRef Van Essen DC, Ugurbil K, Auerbach E, Barch D, Behrens TE, Bucholz R, Chang A, Chen L, Corbetta M, Curtiss SW (2012) The human connectome project: a data acquisition perspective. Neuroimage 62(4):2222–2231PubMedCrossRef
go back to reference Wang H, He W, Wu J, Zhang J, Jin Z, Li L (2019) A coordinate-based meta-analysis of the n-back working memory paradigm using activation likelihood estimation. Brain Cogn 132:1–12PubMedCrossRef Wang H, He W, Wu J, Zhang J, Jin Z, Li L (2019) A coordinate-based meta-analysis of the n-back working memory paradigm using activation likelihood estimation. Brain Cogn 132:1–12PubMedCrossRef
go back to reference Wolf RC, Vasic N, Walter H (2006) Differential activation of ventrolateral prefrontal cortex during working memory retrieval. Neuropsychologia 44(12):2558–2563PubMedCrossRef Wolf RC, Vasic N, Walter H (2006) Differential activation of ventrolateral prefrontal cortex during working memory retrieval. Neuropsychologia 44(12):2558–2563PubMedCrossRef
go back to reference Wu Q, Ripp I, Emch M, Koch K (2021) Cortical and subcortical responsiveness to intensive adaptive working memory training: an mri surface-based analysis. Hum Brain Mapp 42(9):2907–2920PubMedPubMedCentralCrossRef Wu Q, Ripp I, Emch M, Koch K (2021) Cortical and subcortical responsiveness to intensive adaptive working memory training: an mri surface-based analysis. Hum Brain Mapp 42(9):2907–2920PubMedPubMedCentralCrossRef
go back to reference Zylberberg J, Strowbridge BW (2017) Mechanisms of persistent activity in cortical circuits: possible neural substrates for working memory. Annu Rev Neurosci 40:603PubMedPubMedCentralCrossRef Zylberberg J, Strowbridge BW (2017) Mechanisms of persistent activity in cortical circuits: possible neural substrates for working memory. Annu Rev Neurosci 40:603PubMedPubMedCentralCrossRef
Metadata
Title
Using modular connectome-based predictive modeling to reveal brain-behavior relationships of individual differences in working memory
Authors
Huayi Yang
Junjun Zhang
Zhenlan Jin
Pouya Bashivan
Ling Li
Publication date
22-06-2023
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2023
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-023-02666-3

Other articles of this Issue 6/2023

Brain Structure and Function 6/2023 Go to the issue