Reversal of cortical information flow during visual imagery as compared to visual perception

The role of bottom-up and top-down connections during visual perception and the formation of mental images was examined by analyzing high-density EEG recordings of brain activity using two state-of-the-art methods for assessing the directionality of cortical signal flow: state-space Granger causality and dynamic causal modeling. We quantified the directionality of signal flow in an occipito-parieto-frontal cortical network during perception of movie clips versus mental replay of the movies and free visual imagery. Both Granger causality and dynamic causal modeling analyses revealed an increased top-down signal flow in parieto-occipital cortices during mental imagery as compared to visual perception. These results are the first direct demonstration of a reversal of the predominant direction of cortical signal flow during mental imagery as compared to perception.

[1]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[2]  Karl J. Friston Functional integration and inference in the brain , 2002, Progress in Neurobiology.

[3]  Adam Gazzaley,et al.  Diminished Top-Down Control Underlies a Visual Imagery Deficit in Normal Aging , 2011, The Journal of Neuroscience.

[4]  M. Fuchs,et al.  Boundary element method volume conductor models for EEG source reconstruction , 2001, Clinical Neurophysiology.

[5]  Giulio Tononi,et al.  Estimation of Cortical Connectivity From EEG Using State-Space Models , 2010, IEEE Transactions on Biomedical Engineering.

[6]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[7]  Scott Makeig,et al.  Information-based modeling of event-related brain dynamics. , 2006, Progress in brain research.

[8]  G. Edelman,et al.  Reentry and the problem of integrating multiple cortical areas: simulation of dynamic integration in the visual system. , 1992, Cerebral cortex.

[9]  Raymond J. Dolan,et al.  Dynamic causal models of steady-state responses , 2009, NeuroImage.

[10]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[11]  Karl J. Friston,et al.  Analysing connectivity with Granger causality and dynamic causal modelling , 2013, Current Opinion in Neurobiology.

[12]  D. Sagi,et al.  Common mechanisms of visual imagery and perception. , 1995, Science.

[13]  Karl J. Friston,et al.  Where bottom-up meets top-down: neuronal interactions during perception and imagery. , 2004, Cerebral cortex.

[14]  M. Buonocore,et al.  Comparison of the neural basis for imagined writing and drawing , 2007, Human brain mapping.

[15]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.

[16]  S. Bressler,et al.  Frequency decomposition of conditional Granger causality and application to multivariate neural field potential data , 2006, Journal of Neuroscience Methods.

[17]  Karl J. Friston,et al.  DCM for complex-valued data: Cross-spectra, coherence and phase-delays , 2012, NeuroImage.

[18]  Karl J. Friston The labile brain. I. Neuronal transients and nonlinear coupling. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  Z. Pylyshyn Return of the mental image: are there really pictures in the brain? , 2003, Trends in Cognitive Sciences.

[20]  David F. Marks,et al.  New directions for mental imagery research. , 1995 .

[21]  C. Cornoldi,et al.  Cognitive and neuronal processes involved in sequential generation of general and specific mental images , 2009, Psychological research.

[22]  Remo Guidieri Res , 1995, RES: Anthropology and Aesthetics.

[23]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[24]  P. Montague,et al.  Vividness of mental imagery: Individual variability can be measured objectively , 2007, Vision Research.

[25]  Karl J. Friston,et al.  Nonlinear coupling between occipital and motor cortex during motor imagery: A dynamic causal modeling study , 2013, NeuroImage.

[26]  S. Kosslyn,et al.  Brain areas underlying visual mental imagery and visual perception: an fMRI study. , 2004, Brain research. Cognitive brain research.

[27]  G Tononi,et al.  Integrated information theory of consciousness: an updated account. , 2012, Archives italiennes de biologie.

[28]  Karl J. Friston,et al.  Dynamic causal modelling of distributed electromagnetic responses , 2009, NeuroImage.

[29]  Giorgio Ganis,et al.  Visual mental imagery and perception produce opposite adaptation effects on early brain potentials , 2008, NeuroImage.

[30]  D. Tucker,et al.  Transition from cortical slow oscillations of sleep to spike-wave seizures , 2009, Clinical Neurophysiology.

[31]  Karl J. Friston,et al.  Dynamic causal modelling of lateral interactions in the visual cortex , 2013, NeuroImage.

[32]  M. Boly,et al.  Granger Causality Analysis of Steady-State Electroencephalographic Signals during Propofol-Induced Anaesthesia , 2012, PloS one.

[33]  H. Akaike A Bayesian analysis of the minimum AIC procedure , 1978 .

[34]  Miles A Whittington,et al.  A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex , 2006, Proceedings of the National Academy of Sciences.

[35]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[36]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[37]  T. Koenig,et al.  Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  Radoslaw Martin Cichy,et al.  Imagery and perception share cortical representations of content and location. , 2012, Cerebral Cortex.

[39]  S. Kosslyn Mental images and the Brain , 2005, Cognitive neuropsychology.

[40]  A. Seth,et al.  Behaviour of Granger causality under filtering: Theoretical invariance and practical application , 2011, Journal of Neuroscience Methods.

[41]  G. Tononi,et al.  Dreaming and the brain: from phenomenology to neurophysiology , 2010, Trends in Cognitive Sciences.

[42]  Barry D. Van Veen,et al.  Cortical patch basis model for spatially extended neural activity , 2006, IEEE Transactions on Biomedical Engineering.

[43]  A. Ishai,et al.  Distributed neural systems for the generation of visual images , 2000, NeuroImage.

[44]  Frank Tong,et al.  The Functional Impact of Mental Imagery on Conscious Perception , 2008, Current Biology.