Neuroimaging-guided rTMS of the left inferior frontal gyrus interferes with repetition priming

Neuroimaging studies of right-handed normal volunteers under semantic word generation tasks have consistently reported left lateralized activation of the anterior inferior frontal gyrus (ifg) which decreased during task repetition. This repetition-related activation decrease has been interpreted as the neurophysiological correlate of repetition priming, a mechanism of implicit memory for initial semantic processing. We interfered with left lateralized ifg activation, as identified by O-15-water PET activation, using repetitive transcranial magnetic stimulation (rTMS) in five right-handed male normal subjects, once using new (unprimed) nouns and once using known (primed) nouns for the procedure. All five subjects exhibited clear left lateralized activations of the triangular part of the left ifg in the PET studies. In all subjects, reaction time latencies were significantly longer during rTMS over the activation sites in the left ifg as compared to latencies off stimulation. Latencies were not affected during stimulation of the right ifg or over the vertex. These effects were observed within the group and in each individual, only if lists of primed nouns were used in the verb-generation task. In conclusion, these results demonstrate that the anterior part of the left ifg is not only involved in semantic processing, but is also essential for repetition priming on semantic tasks since successful interference with rTMS was only observed if lists of primed words were used for the generation task.

[1]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[2]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[3]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[4]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[5]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[6]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[7]  Karl J. Friston,et al.  Reproducibility of PET Activation Studies: Lessons from a Multi-Center European Experiment EU Concerted Action on Functional Imaging , 1996, NeuroImage.

[8]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

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

[11]  A. Thiel,et al.  Individual Functional Anatomy of Verb Generation , 1996, NeuroImage.

[12]  Amassian Ve,et al.  Relationships between animal and human corticospinal responses. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[13]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[14]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

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

[16]  Karl Herholz,et al.  A Method for Surface-Based Quantification of Functional Data from the Human Cortex , 1998 .

[17]  S. Bestmann,et al.  Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS) , 2001, Neuroreport.

[18]  V E Amassian,et al.  Human cerebral cortical responses to contralateral transcranial stimulation. , 1987, Neurosurgery.

[19]  C. Price The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[20]  E. Achten,et al.  Developing a comprehensive presurgical functional MRI protocol for patients with intractable temporal lobe epilepsy: a pilot study , 2002, Neuroradiology.

[21]  I. Johnsrude,et al.  Somatotopic Representation of Action Words in Human Motor and Premotor Cortex , 2004, Neuron.

[22]  A. Drzezga,et al.  Continuous Transcranial Magnetic Stimulation during Positron Emission Tomography: A Suitable Tool for Imaging Regional Excitability of the Human Cortex , 2001, NeuroImage.

[23]  U Pietrzyk,et al.  An interactive technique for three-dimensional image registration: validation for PET, SPECT, MRI and CT brain studies. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[24]  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.

[25]  J. Binder,et al.  Neuroanatomy of language processing studied with functional MRI. , 1997, Clinical neuroscience.

[26]  K Wienhard,et al.  The ECAT EXACT HR: Performance of a New High Resolution Positron Scanner , 1994, Journal of computer assisted tomography.

[27]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

[28]  K Herholz,et al.  Plasticity of language networks in patients with brain tumors: A positron emission tomography activation study , 2001, Annals of neurology.

[29]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[30]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[31]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Alan C. Evans,et al.  Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. , 1998, Journal of neurophysiology.

[33]  Randy L. Buckner,et al.  Effects of Left Inferior Prefrontal Stimulation on Episodic Memory Formation: A Two-Stage fMRIrTMS Study , 2004, Journal of Cognitive Neuroscience.

[34]  M. Crawford,et al.  Trial-to-trial variability of corticospinal volleys in human subjects. , 1995, Electroencephalography and clinical neurophysiology.

[35]  Richard S. J. Frackowiak,et al.  Noun and verb retrieval by normal subjects. Studies with PET. , 1996, Brain : a journal of neurology.

[36]  J Valls-Solé,et al.  Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. , 1993, Electroencephalography and clinical neurophysiology.

[37]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[38]  P. Matthews,et al.  Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study , 2003, Journal of Cognitive Neuroscience.

[39]  Società Italiana di EEG e neurofisiologia clinica , 1981 .