The Effects of Divided Attention on Encoding- and Retrieval-Related Brain Activity: A PET Study of Younger and Older Adults

Divided attention (DA) disrupts episodic encoding, but has little effect on episodic retrieval. Furthermore, normal aging is associated with episodic memory impairments, and when young adults are made to encode information under DA conditions, their memory performance is reduced and resembles that of old adults working under full attention (FA) conditions. Together, these results suggest a common neurocognitive mechanism by which aging and DA during encoding disrupt memory performance. In the current study, we used PET to investigate younger and older adults' brain activity during encoding and retrieval under FA and DA conditions. In FA conditions, the old adults showed reduced activity in prefrontal regions that younger adults activated preferentially during encoding or retrieval, as well as increased activity in prefrontal regions young adults did not activate. These results indicate that prefrontal functional specificity of episodic memory is reduced by aging. During encoding, DA reduced memory performance, and reduced brain activity in left-prefrontal and medial-temporal lobe regions for both age groups, indicating that DA during encoding interferes with encoding processes that lead to better memory performance. During retrieval, memory performance and retrieval-related brain activity were relatively immune to DA for both age groups, suggesting that DA during retrieval does not interfere with the brain systems necessary for successful retrieval. Finally, left inferior prefrontal activity was reduced similarly by aging and by DA during encoding, suggesting that the behavioral correspondence between these effects is the result of a reduced ability to engage in elaborate encoding operations.

[1]  Richard S. J. Frackowiak,et al.  Neural Correlates of Memory Retrieval during Recognition Memory and Cued Recall , 1998, NeuroImage.

[2]  F. Craik,et al.  The attentional demands of encoding and retrieval in younger and older adults: 1. Evidence from divided attention costs. , 1998, Psychology and aging.

[3]  F. Craik,et al.  On the Transfer of Information from Temporary to Permanent Memory [and Discussion] , 1983 .

[4]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[5]  F. Craik,et al.  Depth of processing and the retention of words , 1975 .

[6]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

[7]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Francis Eustache,et al.  The Functional Neuroanatomy of Episodic Memory: The Role of the Frontal Lobes, the Hippocampal Formation, and Other Areas , 1998, NeuroImage.

[9]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[10]  M. Petrides,et al.  Functional Organization of the Human Frontal Cortex for Mnemonic Processing. , 1995, Annals of the New York Academy of Sciences.

[11]  F. Bookstein,et al.  Neurobehavioral effects of prenatal alcohol: Part II. Partial least squares analysis. , 1989, Neurotoxicology and teratology.

[12]  L. Hasher,et al.  Automatic and effortful processes in memory. , 1979 .

[13]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

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

[15]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[16]  D. Schonfield,et al.  Memory storage and aging. , 1966, Canadian journal of psychology.

[17]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[18]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Buckner Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval , 1996, Psychonomic bulletin & review.

[20]  Karl J. Friston,et al.  A PET study of word finding , 1991, Neuropsychologia.

[21]  F. Craik,et al.  The Effect of Divided Attention on Encoding and Retrieval in Episodic Memory Revealed by Positron Emission Tomography , 2000, Journal of Cognitive Neuroscience.

[22]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[24]  N. Mulligan,et al.  The role of attention during encoding in implicit and explicit memory. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

[25]  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.

[26]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[27]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[28]  B. Winblad,et al.  Brain Activation in Young and Older Adults During Implicit and Explicit Retrieval , 1997, Journal of Cognitive Neuroscience.

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

[30]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[31]  P. Suppes,et al.  Contemporary Developments in Mathematical Psychology , 1976 .

[32]  Fergus I. M. Craik,et al.  A functional account of age differences in memory , 2016 .

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

[34]  Brain Imaging in Clinical Psychiatry , 1998, Neurology.

[35]  Fergus I. M. Craik,et al.  A processing resource account of age differences in recall. , 1982 .

[36]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[37]  A R McIntosh,et al.  General and specific brain regions involved in encoding and retrieval of events: what, where, and when. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Richard C. Atkinson,et al.  Search and decision processes in recognition memory. , 1974 .

[39]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[42]  Alan C. Evans,et al.  Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[45]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[46]  T G Turkington,et al.  Adult age differences in the functional neuroanatomy of verbal recognition memory , 1999, Human brain mapping.

[47]  L L Jacoby,et al.  Automatic versus intentional uses of memory: aging, attention, and control. , 1993, Psychology and aging.

[48]  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.

[49]  R. Cabeza,et al.  Imaging Cognition: An Empirical Review of PET Studies with Normal Subjects , 1997, Journal of Cognitive Neuroscience.

[50]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[51]  Fergus I. M. Craik,et al.  Memory Changes in Normal Aging , 1994 .

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

[53]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Michael D. Kopelman,et al.  The handbook of memory disorders , 1995 .

[55]  Cheryl L. Grady,et al.  Neuroimaging and activation of the frontal lobes. , 1999 .

[56]  A. Dale,et al.  Functional–Anatomic Study of Episodic Retrieval II. Selective Averaging of Event-Related fMRI Trials to Test the Retrieval Success Hypothesis , 1998, NeuroImage.

[57]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[58]  Daniel L. Schacter,et al.  The role of hippocampus and frontal cortex in age‐ related memory changes: a PET study , 1996, Neuroreport.

[59]  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.

[60]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[61]  Leslie G. Ungerleider,et al.  Age-related reductions in human recognition memory due to impaired encoding. , 1995, Science.

[62]  L. Light,et al.  Memory and aging: the role of retrieval processes. , 1981, Psychological bulletin.

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

[64]  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.

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