Test-Retest Reliability of fMRI Brain Activity during Memory Encoding

The mechanisms underlying hemispheric specialization of memory are not completely understood. Functional magnetic resonance imaging (fMRI) can be used to develop and test models of hemispheric specialization. In particular for memory tasks however, the interpretation of fMRI results is often hampered by the low reliability of the data. In the present study we therefore analyzed the test-retest reliability of fMRI brain activation related to an implicit memory encoding task, with a particular focus on brain activity of the medial temporal lobe (MTL). Fifteen healthy subjects were scanned with fMRI on two sessions (average retest interval 35 days) using a commonly applied novelty encoding paradigm contrasting known and unknown stimuli. To assess brain lateralization, we used three different stimuli classes that differed in their verbalizability (words, scenes, fractals). Test-retest reliability of fMRI brain activation was assessed by an intraclass-correlation coefficient (ICC), describing the stability of inter-individual differences in the brain activation magnitude over time. We found as expected a left-lateralized brain activation network for the words paradigm, a bilateral network for the scenes paradigm, and predominantly right-hemispheric brain activation for the fractals paradigm. Although these networks were consistently activated in both sessions on the group level, across-subject reliabilities were only poor to fair (ICCs ≤ 0.45). Overall, the highest ICC values were obtained for the scenes paradigm, but only in strongly activated brain regions. In particular the reliability of brain activity of the MTL was poor for all paradigms. In conclusion, for novelty encoding paradigms the interpretation of fMRI results on a single subject level is hampered by its low reliability. More studies are needed to optimize the retest reliability of fMRI activation for memory tasks.

[1]  Mark E. Bastin,et al.  Single subject fMRI test–retest reliability metrics and confounding factors , 2013, NeuroImage.

[2]  Nick F. Ramsey,et al.  Test–retest reliability of fMRI activation during prosaccades and antisaccades , 2007, NeuroImage.

[3]  Á. Pascual-Leone,et al.  Degree of language lateralization determines susceptibility to unilateral brain lesions , 2002, Nature Neuroscience.

[4]  R. Poldrack,et al.  Memory and the Brain: What's Right and What's Left? , 1998, Cell.

[5]  A. Jansen,et al.  Dominance for language and spatial processing: limited capacity of a single hemisphere , 2005, Neuroreport.

[6]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

[7]  Eric Achten,et al.  Lateralized anterior mesiotemporal lobe activation: semirandom functional MR imaging encoding paradigm in patients with temporal lobe epilepsy--initial experience. , 2005, Radiology.

[8]  Ferath Kherif,et al.  r Human Brain Mapping 32:1602–1614 (2011) r Regional and Hemispheric Determinants of Language Laterality: Implications for Preoperative fMRI , 2022 .

[9]  Determination of crossed language dominance: dissociation of language lateralization within the temporoparietal cortex , 2013, Neurocase.

[10]  Nadim Joni Shah,et al.  The effect of G72 genotype on neural correlates of memory encoding and retrieval , 2010, NeuroImage.

[11]  Kelly O'Keefe,et al.  Reliability of functional magnetic resonance imaging associative encoding memory paradigms in non‐demented elderly adults , 2011, Human brain mapping.

[12]  Klaus Fliessbach,et al.  Material-specific memory processing is related to language dominance , 2007, NeuroImage.

[13]  Judy Illes,et al.  Memory Lateralization in Medial Temporal Lobe Epilepsy Assessed by Functional MRI , 2002, Epilepsia.

[14]  Andrew P. Yonelinas,et al.  The intersubject and intrasubject reproducibility of FMRI activation during three encoding tasks: implications for clinical applications , 2006, Neuroradiology.

[15]  R. Sperling,et al.  Test-retest reliability of memory task functional magnetic resonance imaging in Alzheimer disease clinical trials. , 2011, Archives of neurology.

[16]  Karl J. Friston,et al.  Lateralized Cognitive Processes and Lateralized Task Control in the Human Brain , 2003, Science.

[17]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[18]  Michael B. Miller,et al.  fMRI reliability: Influences of task and experimental design , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[19]  Potential bias in meta-analyses of effect sizes in imaging genetics. , 2013, Schizophrenia bulletin.

[20]  L. Davachi,et al.  Distortion and Signal Loss in Medial Temporal Lobe , 2009, PloS one.

[21]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[22]  Tilo Kircher,et al.  Partial support for ZNF804A genotype‐dependent alterations in prefrontal connectivity , 2013, Human brain mapping.

[23]  J. Beaumont,et al.  Future Research Directions in Laterality , 1997, Neuropsychology Review.

[24]  Interhemispheric dissociation of language regions in a healthy subject. , 2006, Archives of neurology.

[25]  C. Forn,et al.  Memory lateralization with 2 functional MR imaging tasks in patients with lesions in the temporal lobe. , 2006, AJNR. American journal of neuroradiology.

[26]  A. Jansen,et al.  Assessment of verbal memory by fMRI: Lateralization and functional neuroanatomy , 2009, Clinical Neurology and Neurosurgery.

[27]  Michael B. Miller,et al.  How reliable are the results from functional magnetic resonance imaging? , 2010, Annals of the New York Academy of Sciences.

[28]  Keith D. White,et al.  Functional MRI of Language in Aphasia: A Review of the Literature and the Methodological Challenges , 2007, Neuropsychology Review.

[29]  Cathy J. Price,et al.  Lateralization is Predicted by Reduced Coupling from the Left to Right Prefrontal Cortex during Semantic Decisions on Written Words , 2010, Cerebral cortex.

[30]  J. Desmond,et al.  Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. , 2001, Brain : a journal of neurology.

[31]  Stefan Knecht,et al.  The assessment of hemispheric lateralization in functional MRI—Robustness and reproducibility , 2006, NeuroImage.

[32]  J. Gabrieli Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[33]  M. Symms,et al.  The Application of Functional MRI of Memory in Temporal Lobe Epilepsy: A Clinical Review , 2004, Epilepsia.

[34]  R. Kahn,et al.  Language lateralization in schizophrenia, an fMRI study , 2001, Schizophrenia Research.

[35]  Tilo Kircher,et al.  Association of rs1006737 in CACNA1C with alterations in prefrontal activation and fronto‐hippocampal connectivity , 2014, Human brain mapping.

[36]  Alexandra J. Golby,et al.  The brain basis for episodic memory: Insights from functional MRI, intracranial EEG, and patients with epilepsy , 2006, Epilepsy & Behavior.

[37]  Steven C. R. Williams,et al.  Measuring fMRI reliability with the intra-class correlation coefficient , 2009, NeuroImage.

[38]  Klaus Fliessbach,et al.  Retest reliability of reward-related BOLD signals , 2010, NeuroImage.

[39]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.