Nonlinear Changes in Brain Activity During Continuous Word Repetition: An Event-Related Multiparametric Functional MR Imaging Study

BACKGROUND AND PURPOSE: Changes in brain activation as a function of continuous multiparametric word recognition have not been studied before by using functional MR imaging (fMRI), to our knowledge. Our aim was to identify linear changes in brain activation and, what is more interesting, nonlinear changes in brain activation as a function of extended word repetition. MATERIALS AND METHODS: Fifteen healthy young right-handed individuals participated in this study. An event-related extended continuous word-recognition task with 30 target words was used to study the parametric effect of word recognition on brain activation. Word-recognition–related brain activation was studied as a function of 9 word repetitions. fMRI data were analyzed with a general linear model with regressors for linearly changing signal intensity and nonlinearly changing signal intensity, according to group average reaction time (RT) and individual RTs. RESULTS: A network generally associated with episodic memory recognition showed either constant or linearly decreasing brain activation as a function of word repetition. Furthermore, both anterior and posterior cingulate cortices and the left middle frontal gyrus followed the nonlinear curve of the group RT, whereas the anterior cingulate cortex was also associated with individual RT. CONCLUSION: Linear alteration in brain activation as a function of word repetition explained most changes in blood oxygen level–dependent signal intensity. Using a hierarchically orthogonalized model, we found evidence for nonlinear activation associated with both group and individual RTs.

[1]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[2]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

[3]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[4]  R. Coppola,et al.  Specific versus Nonspecific Brain Activity in a Parametric N-Back Task , 2000, NeuroImage.

[5]  G. Mangun,et al.  Successful Verbal Encoding into Episodic Memory Engages the Posterior Hippocampus: A Parametrically Analyzed Functional Magnetic Resonance Imaging Study , 1998, The Journal of Neuroscience.

[6]  Frederik Barkhof,et al.  Parametric fMRI analysis of visual encoding in the human medial temporal lobe , 1999, Hippocampus.

[7]  Frederik Barkhof,et al.  Determination of individual stimulus–response curves in the visual cortex , 2002, Human brain mapping.

[8]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[9]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[10]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[11]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[12]  M. Witter,et al.  Neuropsychology of infarctions in the thalamus: a review , 2000, Neuropsychologia.

[13]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[14]  Alan C. Evans,et al.  Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Florin Dolcos,et al.  Attention-related activity during episodic memory retrieval: a cross-function fMRI study , 2003, Neuropsychologia.

[16]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[17]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[18]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[19]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[20]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[22]  H Garavan,et al.  A midline dissociation between error-processing and response-conflict monitoring , 2003, NeuroImage.

[23]  P Pietrini,et al.  Increasing required neural response to expose abnormal brain function in mild versus moderate or severe Alzheimer's disease: PET study using parametric visual stimulation. , 1998, The American journal of psychiatry.

[24]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  M. Rugg,et al.  Separating the Brain Regions Involved in Recollection and Familiarity in Recognition Memory , 2005, The Journal of Neuroscience.

[26]  A. Yonelinas.  Components of episodic memory: the contribution of recollection and familiarity. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  A. Saykin,et al.  Functional differentiation of medial temporal and frontal regions involved in processing novel and familiar words: an fMRI study. , 1999, Brain : a journal of neurology.

[28]  Jan W. Van Strien,et al.  Changes in brain electrical activity during extended continuous word recognition , 2005, NeuroImage.

[29]  P. Pietrini,et al.  Frequency Variation of a Pattern-Flash Visual Stimulus during PET Differentially Activates Brain from Striate through Frontal Cortex , 1997, NeuroImage.

[30]  Dick J. Veltman,et al.  Parahippocampal Activation during Successful Recognition of Words: A Self-Paced Event-Related fMRI Study , 2001, NeuroImage.

[31]  A. Dale,et al.  Functional–Anatomic Study of Episodic Retrieval II. Selective Averaging of Event-Related fMRI Trials to Test the Retrieval Success Hypothesis , 1998, NeuroImage.

[32]  R. Henson.  Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[33]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[34]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[35]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[36]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[37]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.