The functional roles of prefrontal cortex in episodic memory. I. Encoding.

Functional neuroimaging studies of episodic memory consistently report an association between memory encoding operations and left prefrontal cortex (PFC) activation. Encoding-related activation has been described in dorsolateral, ventrolateral and anterior prefrontal regions. We tested the hypothesis that a specific component of this left PFC activation reflects organizational processes necessary for optimal memory encoding. Subjects underwent PET scans while learning auditorily presented word lists under dual task conditions. The degree to which they were required to organize word lists semantically was systematically varied across three experimental conditions. A task in which words were already organized produced the least degree of left PFC activity whereas a task requiring subjects to generate an organizational structure was associated with maximal activity in this region. This activation was localized to a region just above the inferior frontal sulcus. The functional specificity of this increased activity for organizational processes was tested using a concurrent distracting task known to disrupt these processes. Distraction resulted in a significant attenuation of this activation during the task emphasizing organizational processes but not other encoding tasks. In contrast, the distraction task resulted in reduced activity in a more ventral/anterior PFC region expressed equally for all memory tasks. The findings indicate that a key function of left dorsolateral PFC at encoding relates specifically to the use of executive processes necessary for the creation of an organizational structure. Activity in more ventral and anterior left PFC regions would appear to reflect a less specific component of episodic memory encoding.

[1]  G Mandler,et al.  Directionality and organizational procexsses in paired-associate learning. , 1967, Journal of experimental psychology.

[2]  Arthur L. Benton,et al.  Differential behavioral effects in frontal lobe disease , 1968 .

[3]  B. Milner,et al.  Interhemispheric differences in the localization of psychological processes in man. , 1971, British medical bulletin.

[4]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[5]  E. Tulving Elements of episodic memory , 1983 .

[6]  A. Baddeley,et al.  Attention and retrieval from long-term memory. , 1984 .

[7]  R. Bornstein,et al.  Effects of localized lesions on the Verbal Concept Attainment Test. , 1985, Journal of clinical and experimental neuropsychology.

[8]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[9]  B. G. Rule,et al.  Adult age differences in working memory. , 1989, Psychology and aging.

[10]  E. Warrington,et al.  Cognitive Neuropsychology: A Clinical Introduction , 1990 .

[11]  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.

[12]  Larry L. Jacoby,et al.  Redefining automaticity: Unconscious influences, awareness, and control , 1993 .

[13]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[14]  Brenda Milner,et al.  Strategic search and retrieval inhibition: The role of the frontal lobes , 1993, Neuropsychologia.

[15]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Morris Moscovitch,et al.  Cognitive resources and dual-task interference effects at retrieval in normal people: The role of the frontal lobes and medial temporal cortex. , 1994 .

[18]  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.

[19]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

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

[21]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[22]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[23]  A. Shimamura,et al.  Impaired use of organizational strategies in free recall following frontal lobe damage , 1995, Neuropsychologia.

[24]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  F. Craik,et al.  The effects of divided attention on encoding and retrieval processes in human memory. , 1996, Journal of experimental psychology. General.

[27]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[28]  Anthony R. McIntosh,et al.  Age-Related Differences in Neural Activity during Memory Encoding and Retrieval: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[29]  C. Frith,et al.  The functional neuroanatomy of episodic memory , 1997, Trends in Neurosciences.

[30]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.