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Motor memory consolidation
ABSTRACTS
Motor Memory Consolidation Reza Shadmehr, Ph.D. and Henry H Holcomb, M.D. Depts. of Biomedical Engineering and Radiology, Johns Hopkins School of Medicine, and Maryland Psychiatric Research Center, University of Maryland; Baltimore, MD ; USA Evidence from learning in a variety of subject groups and paradigms, including normal humans and amnesiacs, suggests that memory for certain types of information is initially represented in a temporary and vulnerable format: There is a small window of time in which a variety of interventions, such as induction of electroconvulsive seizures, learning of a related task, or the inhibition of protein synthesis, can cause a loss of recently acquired memory. However, after this time window, intervention has no effect on recall of the information. This transformation of memory has been called consolidation and neuropsychological studies in humans and other primates have identified the medial temporal lobe (MTL) as a site necessary for the process. However, a kind of learning that is not dependent on the MTL is motor learning. Motor practice leads to memories which are retained even in amnesiac patients with large damage to the MTL. Recently, in a series of studies performed by Shadmehr and colleagues (1,2), it was discovered that the storage of motor information also progresses from an early, vulnerable stage to a more consolidated, longterm stage. In these studies, subjects learned to make arm movements while interacting with a novel mechanical environment (3). By changing the properties of the environment, it was deduced that the memory of the motor skill could be interrupted up to 4 hours after completion of practice (2). Beyond this period, the interfering task had little effect. This has raised the possibility that there exists a distinct region in the cerebral hemisphere which, analogous to the MTL, plays a role in consolidation of motor memories. Five subjects participated in a study of motor learning which involved making arm movements while holding a robot manipulandum (3). The robot either produced no forces (null field condition), random forces, or a velocity dependent curl force field. P E T (H2150 bolus method) was used to measure regional cerebral blood flow during 5 conditions: in a null field, in a random field, early learning in the curl field, late learning in the curl field, and learning at 6 hours later in the same curl field. Two scans were taken in each condition. Based on our previous results, it is likely that during the 6 hour period a consolidation process had taken place. Our main result was a significant rCBF reduction in the prefrontal lobe at the 6 hour late learning stage, contrasted with the early and late curl field learning conditions. In a separate study involving 8 subjects learning the same task, a similar number of movements as in this study were performed in the curl field but without the 6 hours separating the 3 learning sessions (4). In that study, no changes were reported in the prefrontal lobe. Therefore, it is likely that the marked prefrontal lobe reduction in rCBF recorded after 6 hours is due to a time dependent memory representation process and not further training per se. Newly acquired information may initially be maintained through sustained neuronal activity in the neocortex. In the case of declarative memory this activity leads to rapid changes in the strength of synapses made by neurons in the neocortex onto structures in the MTL. With time and persistent activity in the MTL neurons, much slower changes take place in the strength of cortico-cortico synapses, effectively producing a long-term, stable memory in the connections among the cells in the neocortex. Pre-frontal regions may play a similar role in initial "binding" of visual-to- motor information; with time this role may lessen as cortico-cortico connections between the visual and motor regions come to represent the learned skill. 1. Shadmehr R, Brashers-Krug T, Mussa-Ivaldi FA (1994) Interference in learning internal models of inverse dynamics in humans. Adv Neural Inf Proc Syst, Tesauro G e t al. (eds.), vol. 7, MIT Press, pp. 1117-1124. 2. Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor learning. Nature, in press. 3. Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14(5):3208-3224. 4. Brashers-Krug T et al. (1996) Different learning abilities in distinct motor areas of the human brain. Science, submitted.
$590
Motor Memory Consolidation Reza Shadmehr, Ph.D. and Henry H Holcomb, M.D. Depts. of Biomedical Engineering and Radiology, Johns Hopkins School of Medicine, and Maryland Psychiatric Research Center, University of Maryland; Baltimore, MD ; USA Evidence from learning in a variety of subject groups and paradigms, including normal humans and amnesiacs, suggests that memory for certain types of information is initially represented in a temporary and vulnerable format: There is a small window of time in which a variety of interventions, such as induction of electroconvulsive seizures, learning of a related task, or the inhibition of protein synthesis, can cause a loss of recently acquired memory. However, after this time window, intervention has no effect on recall of the information. This transformation of memory has been called consolidation and neuropsychological studies in humans and other primates have identified the medial temporal lobe (MTL) as a site necessary for the process. However, a kind of learning that is not dependent on the MTL is motor learning. Motor practice leads to memories which are retained even in amnesiac patients with large damage to the MTL. Recently, in a series of studies performed by Shadmehr and colleagues (1,2), it was discovered that the storage of motor information also progresses from an early, vulnerable stage to a more consolidated, longterm stage. In these studies, subjects learned to make arm movements while interacting with a novel mechanical environment (3). By changing the properties of the environment, it was deduced that the memory of the motor skill could be interrupted up to 4 hours after completion of practice (2). Beyond this period, the interfering task had little effect. This has raised the possibility that there exists a distinct region in the cerebral hemisphere which, analogous to the MTL, plays a role in consolidation of motor memories. Five subjects participated in a study of motor learning which involved making arm movements while holding a robot manipulandum (3). The robot either produced no forces (null field condition), random forces, or a velocity dependent curl force field. P E T (H2150 bolus method) was used to measure regional cerebral blood flow during 5 conditions: in a null field, in a random field, early learning in the curl field, late learning in the curl field, and learning at 6 hours later in the same curl field. Two scans were taken in each condition. Based on our previous results, it is likely that during the 6 hour period a consolidation process had taken place. Our main result was a significant rCBF reduction in the prefrontal lobe at the 6 hour late learning stage, contrasted with the early and late curl field learning conditions. In a separate study involving 8 subjects learning the same task, a similar number of movements as in this study were performed in the curl field but without the 6 hours separating the 3 learning sessions (4). In that study, no changes were reported in the prefrontal lobe. Therefore, it is likely that the marked prefrontal lobe reduction in rCBF recorded after 6 hours is due to a time dependent memory representation process and not further training per se. Newly acquired information may initially be maintained through sustained neuronal activity in the neocortex. In the case of declarative memory this activity leads to rapid changes in the strength of synapses made by neurons in the neocortex onto structures in the MTL. With time and persistent activity in the MTL neurons, much slower changes take place in the strength of cortico-cortico synapses, effectively producing a long-term, stable memory in the connections among the cells in the neocortex. Pre-frontal regions may play a similar role in initial "binding" of visual-to- motor information; with time this role may lessen as cortico-cortico connections between the visual and motor regions come to represent the learned skill. 1. Shadmehr R, Brashers-Krug T, Mussa-Ivaldi FA (1994) Interference in learning internal models of inverse dynamics in humans. Adv Neural Inf Proc Syst, Tesauro G e t al. (eds.), vol. 7, MIT Press, pp. 1117-1124. 2. Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor learning. Nature, in press. 3. Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14(5):3208-3224. 4. Brashers-Krug T et al. (1996) Different learning abilities in distinct motor areas of the human brain. Science, submitted.
$590