Segregated precuneus network and default mode network in naturalistic imaging

A resting-state network centered at the precuneus has been recently proposed as a precuneus network (PCUN) or “parietal memory network”. Due to its spatial adjacency and overlapping with the default mode network (DMN), it is still not consensus to consider PCUN and DMN separately. Whether considering PCUN and DMN as different networks is a critical question that influences our understanding of brain functions and impairments. Previous resting-state studies using multiple methodologies have demonstrated a robust separation of the two networks. However, since there is no gold standard in justifying the functional difference between the networks in resting-state, we still lack of biological evidence to directly support the separation of the two networks. This study compared the responses and functional couplings of PCUN and DMN when participants were watching a movie and examined how the continuity of the movie context modulated the response of the networks. We identified PCUN and DMN in resting-state fMRI of 48 healthy subjects. The networks’ response to a context-rich video and its context-shuffled version was characterized using the variance of temporal fluctuations and functional connectivity metrics. The results showed that (1) scrambling the contextual information altered the fluctuation level of DMN and PCUN in reversed ways; (2) compared to DMN, the FC within PCUN showed significantly higher sensitivity to the contextual continuity; (3) PCUN exhibited a significantly stronger functional network connectivity with the primary visual regions than DMN. These findings provide evidence for the distinct functional roles of PCUN and DMN in processing context-rich information and call for separately considering the functions and impairments of these networks in resting-state studies.

[1]  Mark Mühlau,et al.  Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. , 2014, Schizophrenia bulletin.

[2]  Adrian W. Gilmore,et al.  A parietal memory network revealed by multiple MRI methods , 2015, Trends in Cognitive Sciences.

[3]  Xi-Nian Zuo,et al.  Segregation between the parietal memory network and the default mode network: effects of spatial smoothing and model order in ICA , 2016, bioRxiv.

[4]  Xi-Nian Zuo,et al.  Generalized RAICAR: Discover homogeneous subject (sub)groups by reproducibility of their intrinsic connectivity networks , 2012, NeuroImage.

[5]  Xiaoping Hu,et al.  Ranking and averaging independent component analysis by reproducibility (RAICAR) , 2008, Human brain mapping.

[6]  Catie Chang,et al.  Connectivity trajectory across lifespan differentiates the precuneus from the default network , 2014, NeuroImage.

[7]  V. Menon.  Large-scale brain networks and psychopathology: a unifying triple network model , 2011, Trends in Cognitive Sciences.

[8]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[9]  Jeffrey G. Ojemann,et al.  The parietal memory network activates similarly for true and associative false recognition elicited via the DRM procedure , 2017, Cortex.

[10]  Riitta Hari,et al.  Intersubject consistency of cortical MEG signals during movie viewing , 2014, NeuroImage.

[11]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[12]  Sheng Zhang,et al.  Functional connectivity mapping of the human precuneus by resting state fMRI , 2012, NeuroImage.

[13]  R. Cameron Craddock,et al.  Individual differences in functional connectivity during naturalistic viewing conditions , 2016 .

[14]  Dardo Tomasi,et al.  Structural and functional connectivity of the precuneus and thalamus to the default mode network , 2017, Human brain mapping.

[15]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[16]  David T. Jones,et al.  Cascading network failure across the Alzheimer’s disease spectrum , 2015, Brain : a journal of neurology.

[17]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[18]  Jesper Andersson,et al.  Isolating the retrieval of imagined pictures during episodic memory: activation of the left precuneus and left prefrontal cortex , 2003, NeuroImage.

[19]  Stephen J. Gotts,et al.  Identifying task-general effects of stimulus familiarity in the parietal memory network , 2019, Neuropsychologia.

[20]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Greicius,et al.  Decoding subject-driven cognitive states with whole-brain connectivity patterns. , 2012, Cerebral cortex.

[22]  V. Calhoun,et al.  Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks , 2008, Human brain mapping.

[23]  R. Buckner,et al.  Evidence for the Default Network's Role in Spontaneous Cognition , 2010 .

[24]  J. Suvisaari,et al.  Precuneus functioning differentiates first-episode psychosis patients during the fantasy movie Alice in Wonderland , 2016, Psychological Medicine.

[25]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[26]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[27]  Alexandros Kafkas,et al.  Two separate, but interacting, neural systems for familiarity and novelty detection: A dual‐route mechanism , 2014, Hippocampus.

[28]  Xi-Nian Zuo,et al.  Individual Variability and Test-Retest Reliability Revealed by Ten Repeated Resting-State Brain Scans over One Month , 2015, PloS one.

[29]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[30]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[31]  Tamara Vanderwal,et al.  Inscapes: A movie paradigm to improve compliance in functional magnetic resonance imaging , 2015, NeuroImage.

[32]  X. Zuo,et al.  Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective , 2014, Neuroscience & Biobehavioral Reviews.

[33]  Charles J. Lynch,et al.  The Default Mode Network in Autism. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[34]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[35]  Janice Chen,et al.  Dynamic reconfiguration of the default mode network during narrative comprehension , 2016, Nature Communications.

[36]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[37]  N. Filippini,et al.  Group comparison of resting-state FMRI data using multi-subject ICA and dual regression , 2009, NeuroImage.

[38]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[39]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[40]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[41]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[42]  M. Raichle.  The brain's default mode network. , 2015, Annual review of neuroscience.

[43]  Xi-Nian Zuo,et al.  A Connectome Computation System for discovery science of brain , 2015 .

[44]  Pierrick Coupé,et al.  volBrain: An Online MRI Brain Volumetry System , 2015, Front. Neuroinform..

[45]  Li Fei-Fei,et al.  Neural mechanisms of rapid natural scene categorization in human visual cortex , 2009, Nature.

[46]  Anders M. Dale,et al.  Generalized Laminar Population Analysis (gLPA) for Interpretation of Multielectrode Data from Cortex , 2016, Front. Neuroinform..

[47]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[48]  R. Cameron Craddock,et al.  Individual differences in functional connectivity during naturalistic viewing conditions , 2016, NeuroImage.

[49]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[50]  Adrian W. Gilmore,et al.  Are There Multiple Kinds of Episodic Memory? An fMRI Investigation Comparing Autobiographical and Recognition Memory Tasks , 2017, The Journal of Neuroscience.

[51]  Rafael Malach,et al.  Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. , 2007, Cerebral cortex.

[52]  Mark A Elliott,et al.  Hemodynamic responses in neural circuitries for detection of visual target and novelty: An event‐related fMRI study , 2007, Human brain mapping.

[53]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

[54]  Istvan Molnar-Szakacs,et al.  Beyond superior temporal cortex: intersubject correlations in narrative speech comprehension. , 2008, Cerebral cortex.

[55]  V. Calhoun,et al.  Temporal lobe and “default” hemodynamic brain modes discriminate between schizophrenia and bipolar disorder , 2008, Human brain mapping.

[56]  Yurii B. Shvetsov,et al.  Common Genetic Variation In Cellular Transport Genes and Epithelial Ovarian Cancer (EOC) Risk , 2015, PloS one.