Coordination of multiple memory systems

On the basis of lesions of different brain areas, several neural systems appear to be important for processing information regarding different types of learning and memory. This paper examines the development of pharmacological and neurochemical approaches to multiple memory systems from past studies of modulation of memory formation. The findings suggest that peripheral neuroendocrine mechanisms that regulate memory processing may target their actions toward those neural systems most engaged in the processing of learning and memory. In addition, measurements of acetylcholine release in different memory systems reveals extensive interactions between memory systems, some cooperative and some competitive. These results imply that many neural systems, often characterized as relatively independent, may in fact interact extensively, blurring the dependencies of different memory tasks on specific neural systems.

[1]  C. Destrade,et al.  Improvement of memory for an operant response by post-training glucose in mice , 1988, Behavioural Brain Research.

[2]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[3]  M. Fillenz,et al.  A role for astrocytes in glucose delivery to neurons? , 1996, Developmental neuroscience.

[4]  Norman M Weinberger,et al.  The nucleus basalis and memory codes: Auditory cortical plasticity and the induction of specific, associative behavioral memory , 2003, Neurobiology of Learning and Memory.

[5]  M. Packard Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  P. E. Gold,et al.  Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: effects of microdialysis flow rate, strain, and age. , 1999, Journal of neurochemistry.

[7]  M. Parent,et al.  Increasing acetylcholine levels in the hippocampus or entorhinal cortex reverses the impairing effects of septal GABA receptor activation on spontaneous alternation. , 2000, Learning & memory.

[8]  P. E. Gold,et al.  Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available, conditions. , 2004, Behavioral neuroscience.

[9]  L. Squire,et al.  The Neuropsychology of Memory , 1990 .

[10]  David Benton,et al.  The delivery rate of dietary carbohydrates affects cognitive performance in both rats and humans , 2002, Psychopharmacology.

[11]  S. Craft,et al.  Modulation of memory by insulin and glucose: neuropsychological observations in Alzheimer's disease. , 2004, European journal of pharmacology.

[12]  P. E. Gold,et al.  Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory , 1995, Neuroscience.

[13]  C. Messier Glucose improvement of memory: a review. , 2004, European journal of pharmacology.

[14]  A. R. Lurii︠a︡,et al.  The neuropsychology of memory , 1977 .

[15]  L. Means,et al.  Facilitated single-alternation go, no-go aquisition following hippocampectomy in the rat. , 1970, Journal of comparative and physiological psychology.

[16]  R. Douglas,et al.  The effect of radical hippocampal ablation on acquisition of avoidance response. , 1961 .

[17]  R. J. McDonald,et al.  Information acquired by the hippocampus interferes with acquisition of the amygdala‐based conditioned‐cue preference in the rat , 1995, Hippocampus.

[18]  R. Hughes Effects of glucose on responsiveness to change in young adult and middle-aged rats , 2003, Physiology & Behavior.

[19]  M. Fillenz,et al.  Extracellular Brain Glucose Levels Reflect Local Neuronal Activity: A Microdialysis Study in Awake, Freely Moving Rats , 1992, Journal of neurochemistry.

[20]  B. Westerink,et al.  Do neurotransmitters sampled by brain microdialysis reflect functional release , 1999 .

[21]  P. E. Gold,et al.  Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat , 1998, Brain Research.

[22]  Chris L. S. Coryn,et al.  Short-term memory , 1975 .

[23]  Mark G Packard,et al.  Post‐training reversible inactivation of hippocampus reveals interference between memory systems , 2002, Hippocampus.

[24]  Paul E. Gold,et al.  Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats , 2003, Neurobiology of Learning and Memory.

[25]  P. E. Gold,et al.  Facilitation of time-dependent memory processes with posttrial epinephrine injections. , 1975, Behavioral biology.

[26]  M. Packard,et al.  Amygdala and “emotional” modulation of the relative use of multiple memory systems , 2004, Neurobiology of Learning and Memory.

[27]  L. K. Marriott,et al.  Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning , 2003, Neurobiology of Learning and Memory.

[28]  F. Pavone,et al.  Shuttle-Box Avoidance Learning in Mice: Improvement by Glucose Combined with Stimulant Drugs , 2000, Neurobiology of Learning and Memory.

[29]  J L McGaugh,et al.  Modification of memory storage processes. , 1971, Behavioral science.

[30]  J. D. McGaugh,et al.  Epinephrine modulates long-term retention of an aversively motivated discrimination. , 1986, Behavioral and neural biology.

[31]  N. White,et al.  Contingent and non-contingent actions of sucrose and saccharin reinforcers: Effects on taste preference and memory , 1984, Physiology & Behavior.

[32]  P. E. Gold,et al.  Glucose effects on memory: behavioral and pharmacological characteristics. , 1986, Behavioral and neural biology.

[33]  C. Baratti,et al.  Effects of Posttraining Administration of Glucose on Retention of a Habituation Response in Mice: Participation of a Central Cholinergic Mechanism , 1996, Neurobiology of Learning and Memory.

[34]  L. Squire Memory and Brain , 1987 .

[35]  P. Colombo,et al.  Learning-induced activation of transcription factors among multiple memory systems , 2004, Neurobiology of Learning and Memory.

[36]  E. Tolman,et al.  Studies in spatial learning; place learning versus response learning. , 1946, Journal of experimental psychology.

[37]  Cedric L. Williams,et al.  The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. , 2004, Behavioral neuroscience.

[38]  S M Zola,et al.  Paradoxical facilitation of object reversal learning after transection of the fornix in monkeys. , 1973, Neuropsychologia.

[39]  M. Fillenz,et al.  Extracellular glucose turnover in the striatum of unanaesthetized rats measured by quantitative microdialysis , 1997, The Journal of physiology.

[40]  N. White,et al.  Memory improvement by glucose, fructose, and two glucose analogs: a possible effect on peripheral glucose transport. , 1987, Behavioral and neural biology.

[41]  P. E. Gold,et al.  Fluctuations in Brain Glucose Concentration during Behavioral Testing: Dissociations between Brain Areas and between Brain and Blood , 2001, Neurobiology of Learning and Memory.

[42]  Q. Gu Contribution of acetylcholine to visual cortex plasticity , 2003, Neurobiology of Learning and Memory.

[43]  P. E. Gold,et al.  Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  P. Calabresi,et al.  Dopamine, Acetylcholine and Nitric Oxide Systems Interact to Induce Corticostriatal Synaptic Plasticity , 2003, Reviews in the neurosciences.

[45]  R. J. McDonald,et al.  Dorsal/ventral hippocampus, fornix, and conditioned place preference , 2001, Hippocampus.

[46]  Larry R. Squire,et al.  Neuropsychology of memory, 2nd ed. , 1992 .

[47]  D. Costa-Miserachs,et al.  Posttraining epinephrine and memory consolidation in rats with different basic learning capacities The role of the stria terminalis , 1998, Experimental Brain Research.

[48]  F. Pavone,et al.  Shuttle-Box Avoidance Learning in Mice: Improvement by Combined Glucose and Tacrine , 1998, Neurobiology of Learning and Memory.

[49]  P. E. Gold,et al.  ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: a potential mechanism for glucose-mediated memory enhancement , 1999, Neuroscience.

[50]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[51]  A. Cherkin Kinetics of memory consolidation: role of amnesic treatment parameters. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[52]  P. E. Gold,et al.  Food for thought: fluctuations in brain extracellular glucose provide insight into the mechanisms of memory modulation. , 2002, Behavioral and cognitive neuroscience reviews.

[53]  P. E. Gold,et al.  Intrahippocampal Infusions of K-ATP Channel Modulators Influence Spontaneous Alternation Performance: Relationships to Acetylcholine Release in the Hippocampus , 2001, The Journal of Neuroscience.

[54]  M. Segal,et al.  Muscarinic receptors involved in hippocampal plasticity. , 1997, Life sciences.

[55]  Epinephrine Fails to Enhance Performance of Food-Deprived Rats on a Delayed Spontaneous Alternation Task , 2000, Neurobiology of Learning and Memory.

[56]  D. Korol Enhancing Cognitive Function across the Life Span , 2002, Annals of the New York Academy of Sciences.

[57]  M. Packard,et al.  Amygdala Modulation of Multiple Memory Systems: Hippocampus and Caudate-Putamen , 1998, Neurobiology of Learning and Memory.

[58]  P. E. Gold,et al.  Intra-amygdala infusions of scopolamine impair performance on a conditioned place preference task but not a spatial radial maze task , 1998, Behavioural Brain Research.

[59]  P. E. Gold,et al.  Memory Modulation Across Neural Systems: Intra-Amygdala Glucose Reverses Deficits Caused by Intraseptal Morphine on a Spatial Task But Not on an Aversive Task , 1998, The Journal of Neuroscience.

[60]  Michael E. Ragozzino,et al.  Modulation of Hippocampal Acetylcholine Release and Spontaneous Alternation Scores by Intrahippocampal Glucose Injections , 1998, The Journal of Neuroscience.

[61]  B. Westerink,et al.  Brain microdialysis and its application for the study of animal behaviour , 1995, Behavioural Brain Research.

[62]  H Lund-Andersen,et al.  Transport of glucose from blood to brain. , 1979, Physiological reviews.

[63]  F. Restle Discrimination of cues in mazes: a resolution of the place-vs.-response question. , 1957, Psychological review.

[64]  R. J. McDonald,et al.  Multiple Parallel Memory Systems in the Brain of the Rat , 2002, Neurobiology of Learning and Memory.

[65]  Paul E. Gold Memory modulation roles of peripheral catecholamines , 1984 .

[66]  P. E. Gold Drug enhancement of memory in aged rodents and humans. , 2001 .

[67]  C. Messier Object Recognition in Mice: Improvement of Memory by Glucose , 1997, Neurobiology of Learning and Memory.

[68]  J. Overmier,et al.  Animal research and human health: Advancing human welfare through behavioral science. , 2001 .

[69]  P. Best,et al.  Fimbria/fornix lesions facilitate the learning of a nonspatial response task , 1995, Psychonomic bulletin & review.

[70]  P. E. Gold,et al.  Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. D. McGaugh,et al.  Epinephrine facilitation of appetitive learning: attenuation with adrenergic receptor antagonists. , 1985, Behavioral and neural biology.

[72]  I. Izquierdo,et al.  On brain lesions, the milkman and Sigmunda , 1998, Trends in Neurosciences.

[73]  ME Ragozzino,et al.  Task-dependent effects of intra-amygdala morphine injections: attenuation by intra-amygdala glucose injections , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  P. E. Gold,et al.  Competition between Memory Systems: Acetylcholine Release in the Hippocampus Correlates Negatively with Good Performance on an Amygdala-Dependent Task , 2002, The Journal of Neuroscience.

[75]  T. Bussey,et al.  Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. , 1997, Behavioral neuroscience.

[76]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[77]  M. Packard,et al.  Systemic or intra‐amygdala injections of glucose facilitate memory consolidation for extinction of drug‐induced conditioned reward , 2003, The European journal of neuroscience.

[78]  Michael Davis,et al.  Role of the Amygdala in Fear Extinction Measured with Potentiated Startle , 2003, Annals of the New York Academy of Sciences.

[79]  P. E. Gold,et al.  Switching Memory Systems during Learning: Changes in Patterns of Brain Acetylcholine Release in the Hippocampus and Striatum in Rats , 2003, The Journal of Neuroscience.

[80]  N. Weinberger Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[81]  J L McGaugh,et al.  Time-Dependent Processes in Memory Storage , 1966, Science.

[82]  H. Eichenbaum,et al.  Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. , 1988, Behavioral neuroscience.

[83]  Paul E. Gold,et al.  Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats , 2003, Behavioural Brain Research.

[84]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

[85]  A. Rashidy-pour,et al.  ATP-sensitive potassium channels mediate the effects of a peripheral injection of glucose on memory storage in an inhibitory avoidance task , 2001, Behavioural Brain Research.

[86]  R. Kesner,et al.  Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex , 2004, Experimental Brain Research.

[87]  Larry Cahill,et al.  Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding , 2003, Neurobiology of Learning and Memory.

[88]  Paul E. Gold,et al.  Acetylcholine release in hippocampus and striatum during testing on a rewarded spontaneous alternation task , 2005, Neurobiology of Learning and Memory.

[89]  P. E. Gold Acetylcholine modulation of neural systems involved in learning and memory , 2003, Neurobiology of Learning and Memory.

[90]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[91]  I. Izquierdo,et al.  Cholinergic Neurotransmission and Synaptic Plasticity Concerning Memory Processing , 1997, Neurochemical Research.

[92]  P. E. Gold,et al.  Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. , 2003, Behavioral neuroscience.