Acute effects of alcohol on neural correlates of episodic memory encoding

Although it is well established that alcohol impairs episodic memory encoding, it is unknown how this occurs on a cerebral level. We scanned intoxicated and sober individuals with functional magnetic resonance imaging (fMRI) while they encoded various materials that were recalled the following day. Alcohol impaired memory for object pairs and face-name pairs, but not for words and phrase-word pairs. Impaired performance was associated with reduced bilateral prefrontal activation and non-specific activation of the parahippocampal gyrus. These results suggest that alcohol impairs episodic memory by interfering with activity of regions involved in encoding, and further indicate which regions are critical for human memory.

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

[2]  J. Risberg,et al.  Ethanol Reduces rCFB Activation of Left Dorsolateral Prefrontal Cortex during a Verbal Fluency Task , 2001, Brain and Language.

[3]  E. S. Parker,et al.  Alcohol and Memory: Storage and State Dependency. , 1976 .

[4]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[5]  Seppo Kähkönen,et al.  Alcohol Reduces Prefrontal Cortical Excitability in Humans: A Combined TMS and EEG Study , 2003, Neuropsychopharmacology.

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

[7]  Jerome A. Yesavage,et al.  Gender Differences in Moderate Drinking Effects , 1999, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[8]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[9]  E Tulving,et al.  Recognition failure of words with a single meaning , 1977, Memory & cognition.

[10]  J. Yuille,et al.  Some effects of alcohol on eyewitness memory. , 1990, The Journal of applied psychology.

[11]  H G Wieser,et al.  Human hippocampus associates information in memory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Russell A. Poldrack,et al.  Putting names to faces: Successful encoding of associative memories activates the anterior hippocampal formation , 2003, NeuroImage.

[13]  M. Naveh-Benjamin,et al.  The associative memory deficit of older adults: further support using face-name associations. , 2004, Psychology and aging.

[14]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Coltheart,et al.  358,534 nonwords: The ARC Nonword Database , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

[17]  Anthony Randal McIntosh,et al.  Age-related Changes in Brain Activity across the Adult Lifespan , 2006, Journal of Cognitive Neuroscience.

[18]  Douglas Greve,et al.  Functional MRI detection of pharmacologically induced memory impairment , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  E. S. Parker,et al.  Intact retention in acute alcohol amnesia. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[20]  H. Curran,et al.  Dissociative Effects of Alcohol on Recollective Experience , 1999, Consciousness and Cognition.

[21]  G. Hanks,et al.  The cognitive and psychomotor effects of opioid analgesics , 1995, European Journal of Clinical Pharmacology.

[22]  M. Chee,et al.  Functional Imaging of Working Memory after 24 Hr of Total Sleep Deprivation , 2004, The Journal of Neuroscience.

[23]  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 .

[24]  O. Parsons,et al.  Altered hemispheric functioning under alcohol. , 1977, Journal of studies on alcohol.

[25]  J. Gardiner.  Functional aspects of recollective experience , 1988, Memory & cognition.

[26]  Y Yonekura,et al.  An fMRI study of the functional neuroanatomy of picture encoding in younger and older adults. , 2001, Brain research. Cognitive brain research.

[27]  R. Cabeza,et al.  Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. , 2004, Cerebral cortex.

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

[29]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[30]  Richard J. Haier,et al.  Alcohol induced changes in regional cerebral glucose metabolic rate during divided attention , 1999 .

[31]  P. Rubé,et al.  L’examen Clinique en Psychologie , 1959 .

[32]  L. Bäckman,et al.  Priming and cued recall in elderly, alcohol intoxicated and sleep deprived subjects: a case of functionally similar memory deficits , 1989, Psychological Medicine.

[33]  T. Turkington,et al.  Adult Age Differences in Visual Word Identification: Functional Neuroanatomy by Positron Emission Tomography , 2002, Brain and Cognition.

[34]  D. Schacter,et al.  The neural origins of specific and general memory: the role of the fusiform cortex , 2005, Neuropsychologia.

[35]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[36]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[37]  Nora D. Volkow,et al.  Effects of acute alcohol intoxication on cerebral blood flow measured with PET , 1988, Psychiatry Research.

[38]  A R McIntosh,et al.  The neural correlates of intentional learning of verbal materials: a PET study in humans. , 1996, Brain research. Cognitive brain research.

[39]  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.

[40]  O. Aasland,et al.  Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on Early Detection of Persons with Harmful Alcohol Consumption--II. , 1993, Addiction.

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

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

[43]  P. Roland,et al.  Right prefrontal activation during encoding, but not during retrieval, in a non-verbal paired-associates task. , 1998, Cerebral cortex.

[44]  E. Tulving.  Memory and consciousness. , 1985 .

[45]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[46]  E. S. Parker,et al.  Memory encoding and retrieval on the ascending and descending limbs of the blood alcohol concentration curve , 2005, Psychopharmacology.

[47]  Karl Herholz,et al.  Learning face-name associations and the effect of age and performance: a PET activation study , 2001, Neuropsychologia.

[48]  J. Pekar,et al.  Alcohol Intoxication Effects on Simulated Driving: Exploring Alcohol-Dose Effects on Brain Activation Using Functional MRI , 2004, Neuropsychopharmacology.

[49]  A. Rey.  L'examen clinique in psychologie , 1964 .

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

[51]  J. M. Silvers,et al.  Impairments in spatial learning and memory: ethanol, allopregnanolone, and the hippocampus , 2003, Brain Research Reviews.

[52]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[53]  G. Hanks,et al.  The cognitive and psychomotor effects of opioid analgesics , 1995, European Journal of Clinical Pharmacology.

[54]  A. Scheurich,et al.  Acute Alcohol Effects on Neuronal and Attentional Processing: Striatal Reward System and Inhibitory Sensory Interactions under Acute Ethanol Challenge , 2004, Neuropsychopharmacology.

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

[56]  Dick J Veltman,et al.  Common pathway in the medial temporal lobe for storage and recovery of words as revealed by event‐related functional MRI , 2004, Hippocampus.

[57]  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.