Prefrontal cortex asymmetry for memory encoding of words and abstract shapes.

Previous work suggested a differential contribution of prefrontal cortex (PFC) to successful encoding depending on the stimulus material. Here, we tested the hypothesis that encoding of words preferentially involves the left PFC, while encoding of nonverbal items (abstract shapes) relies on the right PFC. We used an experimental design that evaluated encoding of both words and abstract shapes in the same healthy volunteers. A transient virtual lesion of the left or the right PFC was elicited with transcranial magnetic stimulation (TMS) while subjects memorized verbal and nonverbal items. We found that encoding of verbal material was disrupted by left PFC stimulation, whereas encoding of nonverbal material was disrupted by right PFC stimulation. These results demonstrate a functionally relevant lateralization of prefrontal contribution for verbal and nonverbal memory encoding.

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

[2]  M. Rugg,et al.  Task-dependency of the neural correlates of episodic encoding as measured by fMRI. , 2001, Cerebral cortex.

[3]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. Petersen,et al.  Wada Testing Reveals Frontal Lateralization for the Memorization of Words and Faces , 2002, Journal of Cognitive Neuroscience.

[5]  L. Squire.  "Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans": Correction. , 1992 .

[6]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

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

[8]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[9]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[10]  G. C. Orden,et al.  Word identification in reading proceeds from spelling to sound to meaning. , 1988, Journal of experimental psychology. Learning, memory, and cognition.

[11]  E. Metter,et al.  Verbal and nonverbal recognition memory in aphasic and nonaphasic stroke patients , 1980, Brain and Language.

[12]  J. Rothwell,et al.  Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity , 2000, Current Opinion in Neurobiology.

[13]  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.

[14]  Peter J. Whitehouse,et al.  Imagery and verbal encoding in left and right hemisphere damaged patients , 1981, Brain and Language.

[15]  J. Fiez.  Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[16]  D. Schacter,et al.  When encoding yields remembering: insights from event-related neuroimaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  S. Petersen,et al.  Frontal cortex contributes to human memory formation , 1999, Nature Neuroscience.

[18]  Yasushi Miyashita,et al.  Generation of fractal patterns for probing the visual memory , 1991, Neuroscience Research.

[19]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[20]  N. J. Cohen,et al.  Different Memory Systems Underlying Acquisition of Procedural and Declarative Knowledge a , 1985, Annals of the New York Academy of Sciences.

[21]  Y. Miyashita.  Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[22]  P. Goldman-Rakic.  Architecture of the Prefrontal Cortex and the Central Executive , 1995, Annals of the New York Academy of Sciences.

[23]  Gurindar S. Sohi,et al.  Memory systems , 1996, CSUR.

[24]  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.

[25]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[26]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[27]  Philippe A. Chouinard,et al.  Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. , 2003, Journal of neurophysiology.

[28]  H. Sackeim,et al.  Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials , 2001, Biological Psychiatry.

[29]  Shoogo Ueno,et al.  Asymmetries of prefrontal cortex in human episodic memory: effects of transcranial magnetic stimulation on learning abstract patterns , 2002, Neuroscience Letters.

[30]  Anthony D Wagner,et al.  Memory orientation and success: separable neurocognitive components underlying episodic recognition , 2003, Neuropsychologia.

[31]  Michael Petrides,et al.  Behavioural effects of frontal-lobe lesions in man , 1984, Trends in Neurosciences.

[32]  Toma S Pauss.  Imaging the brain before \ during \ and after transcranial magnetic stimulation , 2022 .

[33]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[34]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  B. Milner,et al.  Frontal lobes and the temporal organization of memory. , 1985, Human neurobiology.

[36]  M. Hallett.  Transcranial magnetic stimulation and the human brain , 2000, Nature.

[37]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[38]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[39]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[40]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[41]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[42]  Carlo Miniussi,et al.  The Role of Prefrontal Cortex in Verbal Episodic Memory: rTMS Evidence , 2003, Journal of Cognitive Neuroscience.

[43]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[44]  A. Baddeley.  The concept of episodic memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[45]  P. Schwanenflugel,et al.  Context availability and the recall of abstract and concrete words , 1992, Memory & cognition.

[46]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[47]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.