The neurobiology of learning and memory
29 Aug 1986-Science (American Association for the Advancement of Science)-Vol. 233, Iss: 4767, pp 941-947
TL;DR: Probably applications of this new understanding of the neural bases of learning and memory range from education to the treatment of learning disabilities to the design of new artificial intelligence systems.
Abstract: Study of the neurobiology of learning and memory is in a most exciting phase. Behavioral studies in animals are characterizing the categories and properties of learning and memory; essential memory trace circuits in the brain are being defined and localized in mammalian models; work on human memory and the brain is identifying neuronal systems involved in memory; the neuronal, neurochemical, molecular, and biophysical substrates of memory are beginning to be understood in both invertebrate and vertebrate systems; and theoretical and mathematical analysis of basic associative learning and of neuronal networks in proceeding apace. Likely applications of this new understanding of the neural bases of learning and memory range from education to the treatment of learning disabilities to the design of new artificial intelligence systems.
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TL;DR: The best understood form of long-term potentiation is induced by the activation of the N-methyl-d-aspartate receptor complex, which allows electrical events at the postsynaptic membrane to be transduced into chemical signals which, in turn, are thought to activate both pre- and post Synaptic mechanisms to generate a persistent increase in synaptic strength.
Abstract: Long-term potentiation of synaptic transmission in the hippocampus is the primary experimental model for investigating the synaptic basis of learning and memory in vertebrates. The best understood form of long-term potentiation is induced by the activation of the N-methyl-D-aspartate receptor complex. This subtype of glutamate receptor endows long-term potentiation with Hebbian characteristics, and allows electrical events at the postsynaptic membrane to be transduced into chemical signals which, in turn, are thought to activate both pre- and postsynaptic mechanisms to generate a persistent increase in synaptic strength.
11,123 citations
TL;DR: The role of the hippocampus is considered, which is needed temporarily to bind together distributed sites in neocortex that together represent a whole memory.
Abstract: This article considers the role of the hippocampus in memory function. A central thesis is that work with rats, monkeys, and humans--which has sometimes seemed to proceed independently in 3 separate literatures--is now largely in agreement about the function of the hippocampus and related structures. A biological perspective is presented, which proposes multiple memory systems with different functions and distinct anatomical organizations. The hippocampus (together with anatomically related structures) is essential for a specific kind of memory, here termed declarative memory (similar terms include explicit and relational). Declarative memory is contrasted with a heterogeneous collection of nondeclarative (implicit) memory abilities that do not require the hippocampus (skills and habits, simple conditioning, and the phenomenon of priming). The hippocampus is needed temporarily to bind together distributed sites in neocortex that together represent a whole memory.
5,283 citations
TL;DR: In this article, a method for clinical description and classification of both normal and abnormal personality variants is proposed based on a general biosocial theory of personality, and three dimensions of personality are defined in terms of the basic stimulus-response characteristics of novelty seeking, harm avoidance and reward dependence.
Abstract: • A systematic method for clinical description and classification of both normal and abnormal personality variants is proposed based on a general biosocial theory of personality. Three dimensions of personality are defined in terms of the basic stimulus-response characteristics of novelty seeking, harm avoidance, and reward dependence. The possible underlying genetic and neuroanatomical bases of observed variation in these dimensions are reviewed and considered in relation to adaptive responses to environmental challenge. The functional interaction of these dimensions leads to integrated patterns of differential response to novelty, punishment, and reward. The possible tridimensional combinations of extreme (high or low) variants on these basic stimulusresponse characteristics correspond closely to traditional descriptions of personality disorders. This reconciles dimensional and categorical approaches to personality description. It also implies that the underlying structure of normal adaptive traits is the same as that of maladaptive personality traits, except for schizotypal and paranoid disorders.
3,329 citations
TL;DR: The medial temporal lobe memory system is needed to bind together the distributed storage sites in neocortex that represent a whole memory, but the role of this system is only temporary, as time passes after learning, memory stored in neoc cortex gradually becomes independent of medialporal lobe structures.
Abstract: Studies of human amnesia and studies of an animal model of human amnesia in the monkey have identified the anatomical components of the brain system for memory in the medial temporal lobe and have illuminated its function. This neural system consists of the hippocampus and adjacent, anatomically related cortex, including entorhinal, perirhinal, and parahippocampal cortices. These structures, presumably by virtue of their widespread and reciprocal connections with neocortex, are essential for establishing long-term memory for facts and events (declarative memory). The medial temporal lobe memory system is needed to bind together the distributed storage sites in neocortex that represent a whole memory. However, the role of this system is only temporary. As time passes after learning, memory stored in neocortex gradually becomes independent of medial temporal lobe structures.
3,096 citations
TL;DR: In this paper, three dimensions of personality have been described that may reflect individual differences in brain systems modulating the activation, maintenance, and inhibition of behavioral responses to the effects of alcohol and other environmental stimuli.
Abstract: Clinical, genetic, and neuropsychopharmacological studies of developmental factors in alcoholism are providing a better understanding of the neurobiological bases of personality and learning. Studies of the adopted-away children of alcoholics show that the predisposition to initiate alcohol-seeking behavior is genetically different from susceptibility to loss of control after drinking begins. Alcohol-seeking behavior is a special case of exploratory appetitive behavior and involves different neurogenetic processes than do susceptibility to behavioral tolerance and dependence on the antianxiety or sedative effects of alcohol. Three dimensions of personality have been described that may reflect individual differences in brain systems modulating the activation, maintenance, and inhibition of behavioral responses to the effects of alcohol and other environmental stimuli. These personality traits distinguish alcoholics with different patterns of behavioral, neurophysiological, and neuropharmacological responses to alcohol.
2,246 citations
References
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TL;DR: The after‐effects of repetitive stimulation of the perforant path fibres to the dentate area of the hippocampal formation have been examined with extracellular micro‐electrodes in rabbits anaesthetized with urethane.
Abstract: 1. The after-effects of repetitive stimulation of the perforant path fibres to the dentate area of the hippocampal formation have been examined with extracellular micro-electrodes in rabbits anaesthetized with urethane.2. In fifteen out of eighteen rabbits the population response recorded from granule cells in the dentate area to single perforant path volleys was potentiated for periods ranging from 30 min to 10 hr after one or more conditioning trains at 10-20/sec for 10-15 sec, or 100/sec for 3-4 sec.3. The population response was analysed in terms of three parameters: the amplitude of the population excitatory post-synaptic potential (e.p.s.p.), signalling the depolarization of the granule cells, and the amplitude and latency of the population spike, signalling the discharge of the granule cells.4. All three parameters were potentiated in 29% of the experiments; in other experiments in which long term changes occurred, potentiation was confined to one or two of the three parameters. A reduction in the latency of the population spike was the commonest sign of potentiation, occurring in 57% of all experiments. The amplitude of the population e.p.s.p. was increased in 43%, and of the population spike in 40%, of all experiments.5. During conditioning at 10-20/sec there was massive potentiation of the population spike (;frequency potentiation'). The spike was suppressed during stimulation at 100/sec. Both frequencies produced long-term potentiation.6. The results suggest that two independent mechanisms are responsible for long-lasting potentiation: (a) an increase in the efficiency of synaptic transmission at the perforant path synapses; (b) an increase in the excitability of the granule cell population.
7,008 citations
TL;DR: A detailed theory of cerebellar cortex is proposed whose consequence is that the cerebellum learns to perform motor skills and two forms of input—output relation are described, both consistent with the cortical theory.
Abstract: 1.
A detailed theory of cerebellar cortex is proposed whose consequence is that the cerebellum learns to perform motor skills. Two forms of input-output relation are described, both consistent with the cortical theory. One is suitable for learning movements (actions), and the other for learning to maintain posture and balance (maintenance reflexes).
2.
It is known that the cells of the inferior olive and the cerebellar Purkinje cells have a special one-to-one relationship induced by the climbing fibre input. For learning actions, it is assumed that:
(a)
each olivary cell responds to a cerebral instruction for an elemental movement. Any action has a defining representation in terms of elemental movements, and this representation has a neural expression as a sequence of firing patterns in the inferior olive; and
(b)
in the correct state of the nervous system, a Purkinje cell can initiate the elemental movement to which its corresponding olivary cell responds.
3.
Whenever an olivary cell fires, it sends an impulse (via the climbing fibre input) to its corresponding Purkinje cell. This Purkinje cell is also exposed (via the mossy fibre input) to information about the context in which its olivary cell fired; and it is shown how, during rehearsal of an action, each Purkinje cell can learn to recognize such contexts. Later, when the action has been learnt, occurrence of the context alone is enough to fire the Purkinje cell, which then causes the next elemental movement. The action thus progresses as it did during rehearsal.
4.
It is shown that an interpretation of cerebellar cortex as a structure which allows each Purkinje cell to learn a number of contexts is consistent both with the distributions of the various types of cell, and with their known excitatory or inhibitory natures. It is demonstrated that the mossy fibre-granule cell arrangement provides the required pattern discrimination capability.
5.
The following predictions are made.
(a)
The synapses from parallel fibres to Purkinje cells are facilitated by the conjunction of presynaptic and climbing fibre (or post-synaptic) activity. Reprinted with permission of The Physiological Society, Oxford, England.
(b)
No other cerebellar synapses are modifiable.
(c)
Golgi cells are driven by the greater of the inputs from their upper and lower dendritic fields.
6.
For learning maintenance reflexes, 2(a) and 2 (b) are replaced by 2’. Each olivary cell is stimulated by one or more receptors, all of whose activities are usually reduced by the results of stimulating the corresponding Purkinje cell.
7.
It is shown that if (2’) is satisfied, the circuit receptor → olivary cell → Purkinje cell → effector may be regarded as a stabilizing reflex circuit which is activated by learned mossy fibre inputs. This type of reflex has been called a learned conditional reflex, and it is shown how such reflexes can solve problems of maintaining posture and balance.
8.
5(a), and either (2) or (2’) are essential to the theory: 5(b) and 5(c) are not absolutely essential, and parts of the theory could survive the disproof of either.
3,151 citations
TL;DR: It is demonstrated that, in order for the learning process to be stable, pattern storage must be accomplished principally by weakening synaptic weights rather than by strengthening them.
Abstract: A comprehensive theory of cerebellar function is presented, which ties together the known anatomy and physiology of the cerebellum into a pattern-recognition data processing system. The cerebellum is postulated to be functionally and structurally equivalent to a modification of the classical Perceptron pattern-classification device. It is suggested that the mossy fiber → granule cell → Golgi cell input network performs an expansion recoding that enhances the pattern-discrimination capacity and learning speed of the cerebellar Purkinje response cells. Parallel fiber synapses of the dendritic spines of Purkinje cells, basket cells, and stellate cells are all postulated to be specifically variable in response to climbing fiber activity. It is argued that this variability is the mechanism of pattern storage. It is demonstrated that, in order for the learning process to be stable, pattern storage must be accomplished principally by weakening synaptic weights rather than by strengthening them.
2,449 citations
TL;DR: An apparatus for cleaning and sterilizing objects, such as pharmaceutical caps, plugs and the like, includes an autoclave chamber and a cleaning device having a cleaning drum mounted for a free rotation on a frame.
Abstract: An apparatus for cleaning and sterilizing objects, such as pharmaceutical caps, plugs and the like includes an autoclave chamber and a cleaning device having a cleaning drum mounted for a free rotation on a frame. The frame runs on rollers and can be moved in and out of the autoclave chamber. The cleaning drum has a hollow shaft provided within the drum with spray nozzles and mounted axially in line with a hollow drive shaft passing through one sidewall of the autoclave chamber free to turn and sealed. The drum shaft and the drive shaft may be coupled together by a coupling device. The frame may be released from the drum introduced into the autoclave chamber so that it is not located during the cleaning process in the autoclave chamber and thus will not constitute an additional source of contamination.
2,414 citations
TL;DR: It is proposed that the hippocampus is selectively involved in behaviors that require working memory, irrespective of the type of material (spatial or nonspatial) that is to be processed by that memory.
Abstract: We examine two different descriptions of the behavioral functions of the hippocampal system. One emphasizes spatially organized behaviors, especially those using cognitive maps. The other emphasizes memory, particularly working memory, a short-term memory that requires iexible stimulus-response associations and is highly susceptible to interference. The predictive value of the spatial and memory descriptions were evaluated by testing rats with damage to the hippocampal system in a series of experiments, independently manipulating the spatial and memory characteristics of a behavioral task. No dissociations were found when the spatial characteristics of the stimuli to be remembered were changed; lesions produced a similar deficit in both spatial and nonspatial test procedures, indicating that the hippocampus was similarly involved regardless of the spatial nature of the task. In contrast, a marked dissociation was found when the memory requirements were altered. Rats with lesions were able to perform accurately in tasks that could be solved exclusively on the basis of reference memory. They performed at chance levels and showed no signs of recovery even with extensive postoperative training in tasks that required working memory. In one experiment all the characteristics of the reference memory and working memory procedures were identical except the type of memory required. Consequently, the behavioral dissociation cannot be explained by differences in attention, motivation, response inhibition, or the type of stimuli to be remembered. As a result of these experiments we propose that the hippocampus is selectively involved in behaviors that require working memory, irrespective of the type of material (spatial or nonspatial) that is to be processed by that memory.
2,006 citations