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Network Modularity as a Foundation for Neural Reuse

Published online by Cambridge University Press:  01 January 2022

Abstract

The neural reuse framework developed primarily by Michael Anderson proposes that brain regions are involved in multiple and diverse cognitive tasks and that brain regions flexibly and dynamically interact in different combinations to carry out cognitive functioning. We argue that the evidence cited by Anderson and others falls short of supporting the fundamental principles of neural reuse. We map out this problem and provide solutions by drawing on recent advances in network neuroscience, and we argue that methods employed in network neuroscience provide the means to fully engage in a research program operating under the principles of neural reuse.

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Articles
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Copyright © The Philosophy of Science Association

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References

Achard, S., and Bullmore, E. 2007. “Efficiency and Cost of Economical Brain Functional Networks.” PLoS Computational Biology 3:e17.CrossRefGoogle ScholarPubMed
Anderson, M. L. 2007. “The Massive Redeployment Hypothesis and the Functional Topography of the Brain.” Philosophical Psychology 202:143–74.Google Scholar
Anderson, M. L. 2010. “Neural Reuse: A Fundamental Organizational Principle of the Brain.” Behavioral and Brain Sciences 33:245313.CrossRefGoogle ScholarPubMed
Anderson, M. L. 2015. After Phrenology: Neural Reuse and the Interactive Brain. Cambridge, MA: MIT Press.Google ScholarPubMed
Anderson, M. L. 2016. “Neural Reuse in the Organization and Development of the Brain.” Developmental Medicine and Child Neurology 58:36.CrossRefGoogle ScholarPubMed
Anderson, M. L., Kinnison, J., and Pessoa, L. 2013. “Describing Functional Diversity of Brain Regions and Brain Networks.” Neuroimage 73:5058.CrossRefGoogle ScholarPubMed
Anderson, M. L., and Penner-Wilger, M. 2013. “Neural Reuse in the Evolution and Development of the Brain: Evidence for Developmental Homology?Developmental Psychobiology 55:4251.CrossRefGoogle ScholarPubMed
Anderson, M. L., and Pessoa, L. 2011. “Quantifying the Diversity of Neural Activations in Individual Brain Regions.” Proceedings of the Annual Meeting of the Cognitive Science Society 33:2421–26.Google Scholar
Bassett, D. S., and Bullmore, E. 2006. “Small-World Brain Networks.” Neuroscientist 12:512–23.CrossRefGoogle ScholarPubMed
Bassett, D. S., and Mattar, M. G. 2017. “A Network Neuroscience of Human Learning: Potential to Inform Quantitative Theories of Brain and Behavior.” Trends in Cognitive Sciences 21:250–64.CrossRefGoogle ScholarPubMed
Bassett, D. S., Muzhi, Y., Wymbs, N. F., and Grafton, S. T. 2015. “Learning-Induced Autonomy of Sensorimotor Systems.” Nature Neuroscience 18:744–51.CrossRefGoogle ScholarPubMed
Bassett, D. S., Wymbs, N. F., Porter, M. A., Mucha, P. J., Carlson, J. M., and Grafton, S. T. 2011. “Dynamic Reconfiguration of Human Brain Networks during Learning.” Proceedings of the National Academy of Sciences of the USA 108:7641–46.CrossRefGoogle ScholarPubMed
Bergeron, V. 2007. “Anatomical and Functional Modularity in Cognitive Science: Shifting the Focus.” Philosophical Psychology 20:175–95.CrossRefGoogle Scholar
Bergeron, V. 2016. “Functional Independence and Cognitive Architecture.” British Journal for the Philosophy of Science 67:817–36.CrossRefGoogle Scholar
Blondel, V. D., Guillaume, J.-L., Lambiotte, R., and Lefebvre, E. 2008. “Fast Unfolding of Communities in Large Networks.” Journal of Statistical Mechanics: Theory and Experiment. doi:10.1088/1742-5468/2008/10/P10008.CrossRefGoogle Scholar
Boersma, M., Smit, D. J. A., de Bie, H. M.A., Van Baal, G. C. M., Boomsma, D. I., de Geus, E. J. C., Delemarre-van de Waal, H. A., and Stam, C. J. 2011. “Network Analysis of Resting State EEG in the Developing Young Brain: Structure Comes with Maturation.” Human Brain Mapping 32:413–25.CrossRefGoogle ScholarPubMed
Braun, U., Schafer, A., Walter, H., Erk, S., Romanczuk-Seiferth, N., Haddad, L., Schweiger, J. I., Grimm, O., Heinz, A., Tost, H., Meyer-Lindenberg, A., and Bassett, D. S. 2015. “Dynamic Reconfiguration of Frontal Brain Networks during Executive Cognition in Humans.” Proceedings of the National Academy of Sciences of the USA 112:11678–83.CrossRefGoogle ScholarPubMed
Bullmore, E. T., and Sporns, O. 2009. “Complex Brain Networks: Graph Theoretical Analysis of Structural and Functional Systems.” Nature Reviews Neuroscience 10:186–98.Google ScholarPubMed
Bullmore, E. T., and Sporns, O. 2012. “The Economy of Brain Network Organization.” Nature Neuroscience 13:336–49.Google ScholarPubMed
Burnston, D. C. 2016. “A Contextualist Approach to Functional Localization in the Brain.” Biology and Philosophy 31:124.CrossRefGoogle Scholar
Cao, H., Plichta, M. M., Schäfer, A., Haddad, L., Grimm, O., Schneider, M., Esslinger, C., Kirsch, P., Meyer-Lindenberg, A., and Tost, H. 2014. “Test-Retest Reliability of fMRI-Based Graph Theoretical Properties during Working Memory, Emotion Processing and Resting State.” Neuroimage 84:888900.CrossRefGoogle ScholarPubMed
Cole, M. W., Reynolds, J. R., Power, J. D., Repovs, G., Anticevic, A., and Braver, T. S. 2013. “Multi-Task Connectivity Reveals Flexible Hubs for Adaptive Task Control.” Nature Neuroscience 169:1348–55.Google Scholar
De Brigard, F. 2017. “Cognitive Systems and the Changing Brain.” Philosophical Explorations 202:224–41.Google Scholar
Eguíluz, V. M., Chialvo, D. R., Cecchi, G. A., Baliki, M., and Apkarian, A. V. 2005. “Scale-Free Brain Functional Networks.” Physical Review Letters 94:018102.CrossRefGoogle ScholarPubMed
Felleman, D. J., and Van Essen, D. C. 1991. “Distributed Hierarchical Processing in the Primate Cerebral Cortex.” Cerebral Cortex 1:147.CrossRefGoogle ScholarPubMed
Friston, K. J. 2011. “Functional and Effective Connectivity: A Review.” Brain Connectivity 1:1336.CrossRefGoogle ScholarPubMed
Geib, B. R., Stanley, M. L., Dennis, N. A., Woldorff, M. G., and Cabeza, R. 2017. “From Hippocampus to Whole-Brain: The Role of Integrative Processing in Episodic Memory Retrieval.” Human Brain Mapping 38:2242–49.CrossRefGoogle ScholarPubMed
Geib, B. R., Stanley, M. L., Wing, E. A., Laurienti, P. J., and Cabeza, R. 2015. “Hippocampal Contributions to the Large-Scale Episodic Memory Network Predict Vivid Visual Memories.” Cerebral Cortex 27:680–93.Google Scholar
Gong, G., Yong, H., Concha, L., Lebel, C., Gross, D. W., Evans, A. C., and Beaulieu, C. 2009. “Mapping Anatomical Connectivity Patterns of Human Cerebral Cortex Using In Vivo Diffusion Tensor Imaging Tractography.” Cerebral Cortex 19:524–36.CrossRefGoogle ScholarPubMed
Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., and Sporns, O. 2008. “Mapping the Structural Core of Human Cerebral Cortex.” PLoS Biology 67:e159.CrossRefGoogle Scholar
Hardcastle, V. G., and Stewart, M. 2002. “What Do Brain Data Really Show?Philosophy of Science 69:572–85.CrossRefGoogle Scholar
He, Y., Chen, Z. J., and Evans, A. C. 2007. “Small-World Anatomical Networks in the Human Brain Revealed by Cortical Thickness from MRI.” Cerebral Cortex 17:2407–19.CrossRefGoogle ScholarPubMed
Heitger, M. H., Ronsse, R., Dhollander, T., Dupont, P., Caeyenberghs, K., and Swinnen, S. P. 2012. “Motor Learning-Induced Changes in Functional Brain Connectivity as Revealed by Means of Graph-Theoretical Network Analysis.” Neuroimage 61:633–50.CrossRefGoogle ScholarPubMed
Hermundstad, A. M., Bassett, D. S., Brown, K. S., Aminoff, E. M., Clewett, D., Freeman, S., Frithsen, A., Johnson, A., Tipper, C. M., Miller, M. B., Grafton, S. T., and Carlson, J. M. 2013. “Structural Foundations of Resting-State and Task-Based Functional Connectivity in the Human Brain.” Proceedings of the National Academy of Sciences of the USA 110:6169–74.CrossRefGoogle ScholarPubMed
Honey, C. J., Kötter, R., Breakspear, M., and Sporns, O. 2007. “Network Structure of Cerebral Cortex Shapes Functional Connectivity on Multiple Time Scales.” Proceedings of the National Academy of Sciences of the USA 104:10240–45.CrossRefGoogle ScholarPubMed
Honey, C. J., Thivierge, J.-P., and Sporns, O. 2010. “Can Structure Predict Function in the Human Brain?Neuroimage 52:766–76.CrossRefGoogle ScholarPubMed
Kanwisher, N., McDermott, J., and Chun, M. M. 1997. “The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception.” Journal of Neuroscience 17:4302–11.CrossRefGoogle ScholarPubMed
Klein, C. 2010. “Philosophical Issues in Neuroimaging.” Philosophy Compass 5:186–98.CrossRefGoogle Scholar
Klein, C. 2012. “Cognitive Ontology and Region- versus Network-Oriented Analyses.” Philosophy of Science 795:952–60.Google Scholar
Maldjian, J. A., Davenport, E. M., and Whitlow, C. T. 2014. “Graph Theoretical Analysis of Resting-State MEG Data: Identifying Interhemispheric Connectivity and the Default Mode.” Neuroimage 96:8894.CrossRefGoogle ScholarPubMed
McCaffrey, J. B. 2015. “The Brain’s Heterogeneous Functional Landscape.” Philosophy of Science 82:1010–22.CrossRefGoogle Scholar
Menon, V., and Uddin, L. Q. 2010. “Saliency, Switching, Attention and Control: A Network Model of Insula Function.” Brain Structure and Function 214:655–67.CrossRefGoogle ScholarPubMed
Meunier, D., Fonlupt, P., Saive, A.-L., Plailly, J., Ravel, N., and Royet, J.-P. 2014. “Modular Structure of Functional Networks in Olfactory Memory.” Neuroimage 95:264–75.CrossRefGoogle ScholarPubMed
Moussa, M. N., Steen, M. R., Laurienti, P. J., and Hayasaka, S. 2012. “Consistency of Network Modules in Resting-State FMRI Connectome Data.” PLoS ONE 7:e44428.CrossRefGoogle ScholarPubMed
Moussa, M. N., Vechlekar, C. D., Burdette, J. H., Steen, M. R., Hugenschmidt, C. E., and Laurienti, P. J. 2011. “Changes in Cognitive State Alter Human Functional Brain Networks.” Frontiers in Human Neuroscience 5:83.CrossRefGoogle ScholarPubMed
Moussa, M. N., Wesley, M. J., Porrino, L. J., Hayasaka, S., Bechara, A., Burdette, J. H., and Laurienti, P. J. 2014. “Age-Related Differences in Advantageous Decision Making Are Associated with Distinct Differences in Functional Community Structure.” Brain Connectivity 4:193202.CrossRefGoogle ScholarPubMed
Mucha, P. J., Richardson, T., Macon, K., Porter, M. A., and Onnela, J.-P. 2010. “Community Structure in Time-Dependent, Multiscale, and Multiplex Networks.” Science 328:876–78.CrossRefGoogle ScholarPubMed
Muldoon, S. F., and Bassett, D. S. 2016. “Network and Multilayer Approaches to Understanding Human Brain Dynamics.” Philosophy of Science 83:710–20.CrossRefGoogle Scholar
Newman, M. E. J. 2006. “Modularity and Community Structure in Networks.” Proceedings of the National Academy of Sciences of the USA 103:8577–82.CrossRefGoogle ScholarPubMed
Paolini, B. M., Laurienti, P. J., Norris, J., and Rajeski, W. J. 2014. “Meal Replacement: Calming the Hot-State Brain Network of Appetite.” Frontiers in Psychology 5:249.CrossRefGoogle ScholarPubMed
Patel, R., Spreng, R. N., and Turner, G. R. 2013. “Functional Brain Changes following Cognitive and Motor Skills Training: A Quantitative Meta-analysis.” Neurorehabilitation and Neural Repair 27:187–99.CrossRefGoogle ScholarPubMed
Pessoa, L. 2014. “Understanding Brain Networks and Brain Organization.” Physics of Life Reviews 11:400435.CrossRefGoogle ScholarPubMed
Rathkopf, C. 2018. “Network Representation and Complex Systems.” Synthese 195 (1): 5578.CrossRefGoogle Scholar
Rubinov, M., and Sporns, O. 2010. “Complex Network Measures of Brain Connectivity: Uses and Interpretations.” Neuroimage 52:1059–69.CrossRefGoogle ScholarPubMed
Sporns, O. 2011. Networks of the Brain. Cambridge, MA: MIT Press.Google Scholar
Sporns, O., and Betzel, R. F. 2016. “Modular Brain Networks.” Annual Review of Psychology 67:613–40.CrossRefGoogle ScholarPubMed
Stam, C. J., Haan, W. de, Daffertshofer, A., Jones, B. F., Manshanden, I., van Cappellen van Walsum, A. M., Montez, T., Verbunt, J. P. A., de Munck, J. C., van Dijk, B. W., Berendse, H. W., and Scheltens, P. 2009. “Graph Theoretical Analysis of Magnetoencephalographic Functional Connectivity in Alzheimer’s Disease.” Brain 132:213–24.CrossRefGoogle ScholarPubMed
Stanley, M. L., Dagenbach, D., Lyday, R. G., Burdette, J. H., and Laurienti, P. J. 2014. “Changes in Global and Regional Modularity Associated with Increasing Working Memory Load.” Frontiers in Human Neuroscience 8:954.CrossRefGoogle ScholarPubMed
Stanley, M. L., and Brigard, F. De. 2016. “Modularity in Network Neuroscience and Neural Reuse.” Behavioral and Brain Sciences 39:2931.CrossRefGoogle ScholarPubMed
Stanley, M. L., Moussa, M. N., Paolini, B. M., Lyday, R. G., Burdette, J. H., and Laurienti, P. J. 2013. “Defining Nodes in Complex Brain Networks.” Frontiers in Computational Neuroscience 7:169.CrossRefGoogle ScholarPubMed
Steen, M., Hayasaka, S., Joyce, K., and Laurienti, P. J. 2011. “Assessing the Consistency of Community Structure in Complex Networks.” Physical Review E 84:016111.Google Scholar
Telesford, Q. K., Lynall, M.-E., Vettel, J., Miller, M. B., Grafton, S. T., and Bassett, D. S. 2016. “Detection of Functional Brain Network Reconfiguration during Task-Driven Cognitive States.” Neuroimage 142:198210.CrossRefGoogle ScholarPubMed
Telesford, Q. K., Simpson, S. L., Burdette, J. H., Hayasaka, S., and Laurienti, P. J. 2011. “The Brain as a Complex System: Using Network Science as a Tool for Understanding the Brain.” Brain Connectivity 1:295308.CrossRefGoogle ScholarPubMed
Valencia, M., Pastor, M. A., Fernández-Seara, M. A., Artieda, J., Martinerie, J., and Chavez, M. 2009. “Complex Modular Structure of Large-Scale Brain Networks.” Chaos 19:023119.CrossRefGoogle ScholarPubMed
van den Heuvel, M. P., and Sporns, O. 2013. “Network Hubs in the Human Brain.” Trends in Cognitive Sciences 17:683–96.CrossRefGoogle ScholarPubMed
Wang, Z., Dai, Z., Gong, G., Zhou, C., and He, Y. 2014. “Understanding Structural-Functional Relationships in the Human Brain: A Large-Scale Network Perspective.” Neuroscientist 21:290305.CrossRefGoogle ScholarPubMed