Bottom-up sensory processing can induce negative BOLD responses and reduce functional connectivity in nodes of the default mode-like network in rats

The default mode network is a large-scale brain network that is active during rest and internally focused states and deactivates as well as desynchronizes during externally oriented (top-down) attention demanding cognitive tasks. However, it is not sufficiently understood if salient stimuli, able to trigger bottom-up attentional processes, could also result in similar reduction of activity and functional connectivity in the DMN. In this study, we investigated whether bottom-up sensory processing could influence the default mode-like network (DMLN) in rats. DMLN activity was examined using block-design visual functional magnetic resonance imaging (fMRI) while its synchronization was investigated by comparing functional connectivity during a resting versus a continuously stimulated brain state by unpredicted light flashes. We demonstrated that the BOLD response in DMLN regions was decreased during visual stimulus blocks and increased during blanks. Furthermore, decreased inter-network functional connectivity between the DMLN and visual networks as well as decreased intra-network functional connectivity within the DMLN was observed during the continuous visual stimulation. These results suggest that triggering of bottom-up attention mechanisms in sedated rats can lead to a cascade similar to top-down orienting of attention in humans and is able to deactivate and desynchronize the DMLN.

[1]  Mc clearn Strain differences in activity of mice. Influence of illumination. , 1960 .

[2]  E. Stein,et al.  Cingulate activation increases dynamically with response speed under stimulus unpredictability. , 2007, Cerebral cortex.

[3]  John D. E. Gabrieli,et al.  Development of deactivation of the default-mode network during episodic memory formation , 2013, NeuroImage.

[4]  L. Timmermann,et al.  The Functional Networks of Prepulse Inhibition: Neuronal Connectivity Analysis Based on FDG-PET in Awake and Unrestrained Rats , 2016, Frontiers in Behavioral Neuroscience.

[5]  Lars Marstaller,et al.  Adaptive contextualization: A new role for the default mode network in affective learning , 2017, Human brain mapping.

[6]  N. Mabbott,et al.  Progress in Molecular Biology and Translational Science , 2017 .

[7]  Peter Fransson,et al.  Assessing the Influence of Different ROI Selection Strategies on Functional Connectivity Analyses of fMRI Data Acquired During Steady-State Conditions , 2011, PloS one.

[8]  Adam J. Schwarz,et al.  Anti-Correlated Cortical Networks of Intrinsic Connectivity in the Rat Brain , 2013, Brain Connect..

[9]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

[10]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[11]  Brian D. Mills,et al.  Large-scale topology and the default mode network in the mouse connectome , 2014, Proceedings of the National Academy of Sciences.

[12]  Andrei Irimia,et al.  Resting-State Functional Connectivity in Autism Spectrum Disorders: A Review , 2017, Front. Psychiatry.

[13]  S. Hyman,et al.  Animal models of neuropsychiatric disorders , 2010, Nature Neuroscience.

[14]  Beatriz Luna,et al.  Strengthening of Top-Down Frontal Cognitive Control Networks Underlying the Development of Inhibitory Control: A Functional Magnetic Resonance Imaging Effective Connectivity Study , 2010, The Journal of Neuroscience.

[15]  Seth R. Jones,et al.  Resting‐state functional connectivity of the rat brain , 2008, Magnetic resonance in medicine.

[16]  Eva H. Telzer,et al.  Contributions of default mode network stability and deactivation to adolescent task engagement , 2018, Scientific Reports.

[17]  C. C. Gaudes,et al.  Periods of rest in fMRI contain individual spontaneous events which are related to slowly fluctuating spontaneous activity , 2013, Human brain mapping.

[18]  B. Luna,et al.  Age related changes in striatal resting state functional connectivity in autism , 2013, Front. Hum. Neurosci..

[19]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[20]  Juan Zhou,et al.  Applications of Resting-State Functional Connectivity to Neurodegenerative Disease. , 2017, Neuroimaging clinics of North America.

[21]  Alessandro Gozzi,et al.  Large-scale functional connectivity networks in the rodent brain , 2016, NeuroImage.

[22]  Annemie Van der Linden,et al.  Early pathologic amyloid induces hypersynchrony of BOLD resting-state networks in transgenic mice and provides an early therapeutic window before amyloid plaque deposition , 2016, Alzheimer's & Dementia.

[23]  Oscar Fontenla-Romero,et al.  Functional Networks , 2009, Encyclopedia of Artificial Intelligence.

[24]  Marleen Verhoye,et al.  Resting State fMRI Reveals Diminished Functional Connectivity in a Mouse Model of Amyloidosis , 2013, PloS one.

[25]  Hyejin Kang,et al.  Maturation of metabolic connectivity of the adolescent rat brain , 2015, eLife.

[26]  Maxim Bazhenov,et al.  Origin of slow spontaneous resting-state neuronal fluctuations in brain networks , 2017, Proceedings of the National Academy of Sciences.

[27]  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.

[28]  H. Lu,et al.  Resting-State Functional Connectivity in Rat Brain , 2005 .

[29]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[30]  John H. Gilmore,et al.  The dynamic reorganization of the default-mode network during a visual classification task , 2013, Front. Syst. Neurosci..

[31]  Darren J Moore,et al.  Genetic mouse models of neurodegenerative diseases. , 2011, Progress in molecular biology and translational science.

[32]  Shella D. Keilholz,et al.  Considerations for resting state functional MRI and functional connectivity studies in rodents , 2015, Front. Neurosci..

[33]  Scott P. Johnson,et al.  Learning by selection: visual search and object perception in young infants. , 2006, Developmental psychology.

[34]  M. Verhoye,et al.  Functional Connectivity fMRI of the Rodent Brain: Comparison of Functional Connectivity Networks in Rat and Mouse , 2011, PloS one.

[35]  M. Verhoye,et al.  Light stimulus frequency dependence of activity in the rat visual system as studied with high-resolution BOLD fMRI. , 2006, Journal of neurophysiology.

[36]  C. Constantinidis,et al.  Bottom-Up and Top-Down Attention , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[37]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[38]  Thomas J. Schnitzer,et al.  Brain Morphological Signatures for Chronic Pain , 2011, PloS one.

[39]  P. McGuire,et al.  Age effects on the default mode and control networks in typically developing children. , 2014, Journal of psychiatric research.

[40]  M. Raichle,et al.  Rat brains also have a default mode network , 2012, Proceedings of the National Academy of Sciences.

[41]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[42]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

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

[44]  Jutta S. Mayer,et al.  Specialization in the default mode: Task‐induced brain deactivations dissociate between visual working memory and attention , 2009, Human brain mapping.

[45]  Craig K. Jones,et al.  Functional networks in the anesthetized rat brain revealed by independent component analysis of resting-state FMRI. , 2010, Journal of neurophysiology.

[46]  Mariel G Kozberg,et al.  Resting-state hemodynamics are spatiotemporally coupled to synchronized and symmetric neural activity in excitatory neurons , 2016, Proceedings of the National Academy of Sciences.

[47]  Yeung Sam Hung,et al.  Task-related functional connectivity dynamics in a block-designed visual experiment , 2015, Front. Hum. Neurosci..

[48]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  G. Orban,et al.  Default Mode of Brain Function in Monkeys , 2011, The Journal of Neuroscience.

[50]  Tie-Qiang Li,et al.  Default Mode Network, Motor Network, Dorsal and Ventral Basal Ganglia Networks in the Rat Brain: Comparison to Human Networks Using Resting State-fMRI , 2015, PloS one.

[51]  Alessandro Gozzi,et al.  Autism-associated 16p11.2 microdeletion impairs prefrontal functional connectivity in mouse and human , 2018, Brain : a journal of neurology.

[52]  Wei Gao,et al.  Task-positive Functional Connectivity of the Default Mode Network Transcends Task Domain , 2015, Journal of Cognitive Neuroscience.

[53]  Christopher P. Pawela,et al.  Modeling of region-specific fMRI BOLD neurovascular response functions in rat brain reveals residual differences that correlate with the differences in regional evoked potentials , 2008, NeuroImage.

[54]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[55]  Alessandro Gozzi,et al.  Functional connectivity hubs of the mouse brain , 2015, NeuroImage.

[56]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[57]  Hanbing Lu,et al.  Resting-state functional MRI reveals altered brain connectivity and its correlation with motor dysfunction in a mouse model of Huntington’s disease , 2017, Scientific Reports.

[58]  Pan Lin,et al.  Dynamic Default Mode Network across Different Brain States , 2017, Scientific Reports.