Measuring functional connectivity during distinct stages of a cognitive task

The inherently multivariate nature of functional brain imaging data affords the unique opportunity to explore how anatomically disparate brain areas interact during cognitive tasks. We introduce a new method for characterizing inter-regional interactions using event-related functional magnetic resonance imaging (fMRI) data. This method's principle advantage over existing analytical techniques is its ability to model the functional connectivity between brain regions during distinct stages of a cognitive task. The method is implemented by using separate covariates to model the activity evoked during each stage of each individual trial in the context of the general linear model (GLM). The resulting parameter estimates (beta values) are sorted according to the stage from which they were derived to form a set of stage-specific beta series. Regions whose beta series are correlated during a given stage are inferred to be functionally interacting during that stage. To validate the assumption that correlated fluctuations in trial-to-trial beta values imply functional connectivity, we applied the method to an event-related fMRI data set in which subjects performed two sequence-tapping tasks. In concordance with previous electrophysiological and fMRI coherence studies, we found that the task requiring greater bimanual coordination induced stronger correlations between motor regions of the two hemispheres. The method was then applied to an event-related fMRI data set in which subjects performed a delayed recognition task. Distinct functional connectivity maps were generated during the component stages of this task, illustrating how important and novel observations of neural networks within the isolated stages of a cognitive task can be obtained.

[1]  D Le Bihan,et al.  The Dorsolateral Prefrontal Cortex (dlpfc) Plays a Key Role in Working Memory (wm). yet Its Precise Contribution , 2022 .

[2]  E. Tulving,et al.  Age‐related differences in effective neural connectivity during encoding and recall , 1997, Neuroreport.

[3]  Leslie G. Ungerleider,et al.  Changes in limbic and prefrontal functional interactions in a working memory task for faces. , 1996, Cerebral cortex.

[4]  M. A. Jeeves,et al.  Bimanual co-ordination in callosal agenesis and partial commissurotomy , 1988, Neuropsychologia.

[5]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  B. Postle,et al.  Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. , 2000, Brain research. Brain research protocols.

[7]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[8]  T. Mima,et al.  Increased Synchronization of Cortical Oscillatory Activities between Human Supplementary Motor and Primary Sensorimotor Areas during Voluntary Movements , 2001, The Journal of Neuroscience.

[9]  J. Fuster Network memory , 1997, Trends in Neurosciences.

[10]  C. Gerloff,et al.  Bimanual coordination and interhemispheric interaction. , 2002, Acta psychologica.

[11]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[12]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[13]  Lee M. Miller,et al.  Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data , 2004, NeuroImage.

[14]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[15]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[16]  P Turski,et al.  Effect of focal and nonfocal cerebral lesions on functional connectivity studied with MR imaging. , 2001, AJNR. American journal of neuroradiology.

[17]  Thomas Dierks,et al.  Dissociation between overt and unconscious face processing in fusiform face area , 2004, NeuroImage.

[18]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[19]  Leslie G. Ungerleider,et al.  Network analysis of cortical visual pathways mapped with PET , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  L. Parsons,et al.  Interregional connectivity to primary motor cortex revealed using MRI resting state images , 1999, Human brain mapping.

[21]  A. E. Schulman,et al.  Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. , 1999, Brain : a journal of neurology.

[22]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[23]  James B. Rowe,et al.  Parahippocampal Reactivation Signal at Retrieval after Interruption of Rehearsal , 2002, The Journal of Neuroscience.

[24]  O. Koenig,et al.  Separable Mechanisms in Face Processing: Evidence from Hemispheric Specialization , 1991, Journal of Cognitive Neuroscience.

[25]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[26]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[27]  P. Brown,et al.  The functional role of interhemispheric synchronization in the control of bimanual timing tasks , 2002, Experimental Brain Research.

[28]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[29]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[30]  B. Biswal,et al.  Simultaneous assessment of flow and BOLD signals in resting‐state functional connectivity maps , 1997, NMR in biomedicine.

[31]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[32]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[33]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[34]  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.

[35]  C. Curtis,et al.  Success and Failure Suppressing Reflexive Behavior , 2003, Journal of Cognitive Neuroscience.

[36]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[37]  V. Haughton,et al.  Functional connectivity in the thalamus and hippocampus studied with functional MR imaging. , 2000, AJNR. American journal of neuroradiology.

[38]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[39]  R. Passingham,et al.  Changes of cortico-striatal effective connectivity during visuomotor learning. , 2002, Cerebral cortex.

[40]  Robert Sekuler,et al.  Corticolimbic Interactions Associated with Performance on a Short-Term Memory Task Are Modified by Age , 2000, The Journal of Neuroscience.

[41]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

[42]  Joseph B. Sala,et al.  Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory , 2003, Neuropsychologia.

[43]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[45]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[46]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[47]  M. D’Esposito,et al.  Temporal isolation of the neural correlates of spatial mnemonic processing with fMRI. , 1999, Brain research. Cognitive brain research.

[48]  Marcia K. Johnson,et al.  Prefrontal activity associated with working memory and episodic long-term memory , 2003, Neuropsychologia.

[49]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[50]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[51]  Karl J. Friston,et al.  Attentional modulation of effective connectivity from V2 to V5/MT in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[52]  T Landis,et al.  Prosopagnosia and agnosia for noncanonical views. An autopsied case. , 1988, Brain : a journal of neurology.

[53]  R. Fisher 014: On the "Probable Error" of a Coefficient of Correlation Deduced from a Small Sample. , 1921 .

[54]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[55]  E Zarahn,et al.  Event-related functional MRI: implications for cognitive psychology. , 1999, Psychological bulletin.

[56]  Bruno Rossion,et al.  The functionally defined right occipital and fusiform “face areas” discriminate novel from visually familiar faces , 2003, NeuroImage.

[57]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[58]  Ingrid S. Johnsrude,et al.  Can Meaningful Effective Connectivities Be Obtained between Auditory Cortical Regions? , 2001, NeuroImage.

[59]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[60]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[61]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[62]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[63]  J J Pekar,et al.  Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information , 2001, Cognitive, affective & behavioral neuroscience.

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

[65]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[66]  B. Postle,et al.  “ What ” — Then — “ Where ” in Visual Working Memory : An Event-Related fMRI Study , 2000 .

[67]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[68]  J. Lurito,et al.  Correlations in Low-Frequency BOLD Fluctuations Reflect Cortico-Cortical Connections , 2000, NeuroImage.

[69]  R. Passingham,et al.  Prefrontal interactions reflect future task operations , 2003, Nature Neuroscience.

[70]  Leslie G. Ungerleider,et al.  Neural Correlates of Visual Working Memory fMRI Amplitude Predicts Task Performance , 2002, Neuron.

[71]  Sharon L. Thompson-Schill,et al.  Models of Functional Organization of the Lateral Prefrontal Cortex in Verbal Working Memory: Evidence in Favor of the Process Model , 2002, Journal of Cognitive Neuroscience.

[72]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.