The Role of Prefrontal Cortex in Verbal Episodic Memory: rTMS Evidence

Long-term, episodic memory processing is supposed to involve the prefrontal cortex asymmetrically. Here we investigate the role of the dorsolateral prefrontal cortex (DLPFC) in encoding and retrieval of semantically related or unrelated word pairs. Subjects were required to perform a task consisting of two parts: a study phase (encoding), in which word pairs were presented, and a test phase (retrieval), during which stimuli previously presented had to be recognized among other stimuli. Consistently with our previous findings using pictures, repetitive transcranial magnetic stimulation (rTMS) had a significant impact on episodic memory. The performance was significantly disrupted when rTMS was applied to the left or right DLPFC during encoding, and to the right DLPFC in retrieval, but only for unrelated word pairs. These results indicate that the nature of the material to be remembered interacts with the encodingretrieval DLPFC asymmetry; moreover, the crucial role of DLPFC is evident only for novel stimuli.

[1]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  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.

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

[4]  Claudio Babiloni,et al.  Prefontal cortex in long-term memory: an “interference” approach using magnetic stimulation , 2001, Nature Neuroscience.

[5]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[6]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[7]  R. Dolan,et al.  The Role of the Right Anterior Prefrontal Cortex in Episodic Retrieval , 2000, NeuroImage.

[8]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[9]  J. Vizmuller-Zocco,et al.  Lessico di frequenza dell'italiano parlato , 1994 .

[10]  R. Dolan,et al.  Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval. , 1996, Brain : a journal of neurology.

[11]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[12]  Remo Job,et al.  Le associazioni verbali PD-DPSS: norme per 294 parole , 2002 .

[13]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E. Tulving,et al.  PET studies of encoding and retrieval: The HERA model , 1996, Psychonomic bulletin & review.

[15]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

[16]  J. Desmond,et al.  Material‐specific lateralization of prefrontal activation during episodic encoding and retrieval , 1998, Neuroreport.

[17]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[18]  H. Müller-Gärtner,et al.  Encoding and retrieval in declarative learning: a positron emission tomography study , 1998, Behavioural Brain Research.

[19]  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.

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

[21]  Simone Rossi,et al.  TMS in cognitive plasticity and the potential for rehabilitation , 2004, Trends in Cognitive Sciences.

[22]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[23]  A. Paivio Mental Representations: A Dual Coding Approach , 1986 .

[24]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[25]  D. Schmidt,et al.  Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study , 1999, Experimental Brain Research.

[26]  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.

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

[28]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[29]  Pura Guil,et al.  Lessico di frequenza dell´italiano parlato. Milano, Etaslibri, 1993. , 1995 .

[30]  A. Friederici,et al.  Functional asymmetry of human prefrontal cortex: encoding and retrieval of verbally and nonverbally coded information. , 2000, Learning & memory.

[31]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[32]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[33]  C D Frith,et al.  Brain activity during memory retrieval. The influence of imagery and semantic cueing. , 1996, Brain : a journal of neurology.

[34]  R. Frackowiak,et al.  The neural systems sustaining face and proper-name processing , 1998, Brain : a journal of neurology.

[35]  Andy C. H. Lee,et al.  Asymmetric frontal activation during episodic memory: the effects of stimulus type on encoding and retrieval , 2000, Neuropsychologia.

[36]  E Tulving,et al.  Functional role of the prefrontal cortex in retrieval of memories: a PET study , 1995, Neuroreport.

[37]  M. Rugg,et al.  Retrieval processing and episodic memory , 2000, Trends in Cognitive Sciences.

[38]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[39]  A. Dale,et al.  Late Onset of Anterior Prefrontal Activity during True and False Recognition: An Event-Related fMRI Study , 1997, NeuroImage.

[40]  Karl J. Friston,et al.  Scanning patients with tasks they can perform , 1999, Human brain mapping.

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

[42]  H. Müller-Gärtner,et al.  Brain systems engaged in encoding and retrieval of word-pair associates independent of their imagery content or presentation modalities , 2002, Neuropsychologia.

[43]  A R McIntosh,et al.  Functional brain maps of retrieval mode and recovery of episodic information , 1995, Neuroreport.

[44]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[45]  R. Dolan,et al.  Brain regions supporting intentional and incidental memory: a PET study , 1997, Neuroreport.

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

[47]  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.

[48]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.