Building Neural Representations of Habits
SciencePublished 26 November 1999
Mandar Jog, Yasuo Kubota, Christopher I. Connolly, Viveka Hillegaart, Ann M. Graybiel
Citations847
SJR quartileQ1
SJR score10.42
SNIP6.62
Generate an AI Snapshot to get a quick, structured summary of this paper.
Study Snapshot
ObjectiveStudy objective
MethodsResearch methodology
PopulationPopulation studied
Sample sizeSample sizes
OutcomesStudy outcomes here
ResultsStudy results comes here
LimitationsResearch study limitations comes here
A concise AI-generated summary of the paper will appear here once you click Generate AI Snapshot.
TL;DR
Large and widely distributed changes in the neuronal activity patterns occurred in the sensorimotor striatum during behavioral acquisition, culminating in task-related activity emphasizing the beginning and end of the automatized procedure.
Abstract
Memories for habits and skills ("implicit or procedural memory") and memories for facts ("explicit or episodic memory") are built up in different brain systems and are vulnerable to different neurodegenerative disorders in humans. So that the striatum-based mechanisms underlying habit formation could be studied, chronic recordings from ensembles of striatal neurons were made with multiple tetrodes as rats learned a T-maze procedural task. Large and widely distributed changes in the neuronal activity patterns occurred in the sensorimotor striatum during behavioral acquisition, culminating in task-related activity emphasizing the beginning and end of the automatized procedure. The new ensemble patterns remained stable during weeks of subsequent performance of the same task. These results suggest that the encoding of action in the sensorimotor striatum undergoes dynamic reorganization as habit learning proceeds.
Keywords
Neuroscience
ScienceA Neural Substrate of Prediction and Reward
9,610 Citations1997Wolfram Schultz, Peter Dayan +1 more
Findings in this work indicate that dopaminergic neurons in the primate whose fluctuating output apparently signals changes or errors in the predictions of future salient and rewarding events can be understood through quantitative theories of adaptive optimizing control.
Trends in NeurosciencesThe functional anatomy of basal ganglia disorders
5,362 Citations1989Roger L. Albin, Anne B. Young +1 more
A model in which specific types of basal ganglia disorders are associated with changes in the function of subpopulations of striatal projection neurons is proposed, which suggests that the activity of sub Populations of Striatal projections neurons is differentially regulated by striatal afferents and that different striatal projections may mediate different aspects of motor control.
Journal of NeurophysiologyPredictive Reward Signal of Dopamine Neurons
4,582 Citations1998Wolfram Schultz
Dopamine systems may have two functions, the phasic transmission of reward information and the tonic enabling of postsynaptic neurons.
Trends in NeurosciencesPrimate models of movement disorders of basal ganglia origin
3,808 Citations1990Mahlon R. DeLong
This paper describes the changes in neuronal activity in the motor circuit in animal models of hypo- and hyperkinetic disorders and postulates specific disturbances within the basal ganglia-thalamocortical 'motor' circuit.
ScienceDynamics of the Hippocampal Ensemble Code for Space
2,409 Citations1993Matthew A. Wilson, Bruce L. McNaughton
Parallel recording methods outlined here make possible the study of the dynamics of neuronal interactions during unique behavioral events, which suggests that new spatial information creates conditions in the hippocampal circuitry that are conducive to the synaptic modification presumed to be involved in learning.
Annual Review of NeuroscienceCORTICAL PLASTICITY: From Synapses to Maps
2,099 Citations1998Dean V. Buonomano, Michael M. Merzenich
The goal of the current paper is to review the fields of both synaptic and cortical map plasticity with an emphasis on the work that attempts to unite both fields, to highlight the gaps in the understanding of synaptic and cellular mechanisms underlying cortical representational plasticity.
ScienceA Neostriatal Habit Learning System in Humans
1,802 Citations1996Barbara J. Knowlton, Jennifer A. Mangels +1 more
This double dissociation shows that the limbic-diencephalic regions damaged in amnesia and the neostriatum damaged in Parkinson's disease support separate and parallel learning systems.
Neurobiology of Learning and MemoryInactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning
1,515 Citations1996Mark G. Packard, James L. McGaugh
The findings indicate: (1) the hippocampus and caudate nucleus selectively mediate expression of place and response learning, respectively, and in a visually cued extramaze environment, hippocampal-dependent place learning is acquired faster than caUDate-dependent response learning.
Proceedings of the National Academy of SciencesThe acquisition of skilled motor performance: Fast and slow experience-driven changes in primary motor cortex
1,403 Citations1998Avi Karni, Gundela Meyer +5 more
It is shown that a few minutes of daily practice on a sequential finger opposition task can be sufficient to trigger performance gains that require time to become evident, and proposed that skilled motor performance is acquired in several stages: "fast" learning, an initial, within-session improvement phase, followed by a period of consolidation of several hours duration, and then "slow" learnings, consisting of delayed, incremental gains in performance emerging after continued practice.
NeuroscienceThe organization of the projection from the cerebral cortex to the striatum in the rat
1,331 Citations1989Archibald J. McGeorge, Richard L. M. Faull
The detailed organization of the corticostriate projection has been investigated in the brain of the rat using the technique of retrograde transport of horseradish peroxidase following the placement of small, iontophoretic injections.
ScienceThe Basal Ganglia and Adaptive Motor Control
1,325 Citations1994Ann M. Graybiel, Toshihiko Aosaki +2 more
The basal ganglia are neural structures within the motor and cognitive control circuits in the mammalian forebrain and are interconnected with the neocortex by multiple loops that have a distributed modular architecture resembling local expert architectures of computational learning models during sensorimotor learning.
Behavioral NeuroscienceA triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
1,054 Citations2013Robert J. McDonald, Norman M. White
The results of this study are consistent with the hypothesis that the mammalian brain may be capable of acquiring different kinds of information with different, more-or-less independent neural systems.
Neurobiology of Learning and MemoryThe Basal Ganglia and Chunking of Action Repertoires
1,047 Citations1998Ann M. Graybiel
It is proposed that one aspect of basal ganglia-based learning is the recoding of cortically derived information within the striatum that can chunk the representations of motor and cognitive action sequences so that they can be implemented as performance units.
ScienceNeural Correlates of Motor Memory Consolidation
1,034 Citations1997Reza Shadmehr, Henry H. Holcomb
Functional imaging of the brain demonstrates that within 6 hours after completion of practice, while performance remains unchanged, the brain engages new regions to perform the task; there is a shift from prefrontal regions of the cortex to the premotor, posterior parietal, and cerebellar cortex structures, specific to recall of an established motor skill.
NeuronNeuroscience of Addiction
1,029 Citations1998George F. Koob, Pietro Paolo Sanna +1 more
This is publication number 11130-NP from The Scripps Research Institute and research was supported by National Institutes of Health grants DA04043, DA04398, and DA08467.
Behavioral BiologyThe hippocampus and contextual retrieval of information from memory: A theory
962 Citations1974Richard F. Hirsh
A theory which holds that information is normally stored within a specialized memory rather than the system immediately responsible for the performance of behavior is advanced and the effects of hippocampal ablation are explained in terms of the elimination of such transfer.
Journal of Neuroscience MethodsTetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex
757 Citations1995Charles M. Gray, Pedro Maldonado +2 more
Tetrode recording currently provides the best and most reliable method for the isolation of multiple single units in the neocortex using a single probe.
Archives of General PsychiatrySystematic Changes in Cerebral Glucose Metabolic Rate After Successful Behavior Modification Treatment of Obsessive-Compulsive Disorder
688 Citations1996Jeffrey M. Schwartz
Findings in this study replicate and extend previous findings of changes in caudate nucleus function with behavior therapy for obsessive-compulsive disorder.
Nature NeuroscienceExpectation of reward modulates cognitive signals in the basal ganglia
642 Citations1998Reiko Kawagoe, Yoriko Takikawa +1 more
The results indicate that the caudate contributes to the determination of oculomotor outputs by connecting motivational values (for example, expectation of reward) to visual information.
Journal of NeuroscienceResponses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning
611 Citations1994Toshihiko Aosaki, Hiroshi Tsubokawa +4 more
It is concluded that, during the acquisition of a sensorimotor association, TANs widely distributed through the striatum become responsive to sensory stimuli that induce conditioned behavior.
Journal of NeurophysiologyFunctional properties of monkey caudate neurons. III. Activities related to expectation of target and reward
583 Citations1989Okihide Hikosaka, Masahiro Sakamoto +1 more
The present results, together with those in the preceding papers, indicate that the activities of individual caudate neurons--sensory, motor, or cognitive--are dependent on specific contexts of learned behavior.
Current Opinion in NeurobiologyBuilding action repertoires: memory and learning functions of the basal ganglia
563 Citations1995Ann M. Graybiel
Experimental findings on reward-based learning suggest that neural activity in the striatum and substantia nigra, pars compacta changes during behavioral learning, and new evidence also suggests extreme specificity in the neural connections interrelating the basal ganglia, cerebral cortex and thalamus.
Proceedings of the National Academy of SciencesThe effects of practice on the functional anatomy of task performance
535 Citations1998Steven E. Petersen, Hanneke I. Van Mier +2 more
The effects of practice on the functional anatomy observed in two different tasks, a verbal and a motor task, are reviewed and a "scaffolding-storage" framework is interpreted, possibly representing storage of particular associations or capabilities that allow for skilled performance.
BrainDISTURBANCE OF SEQUENTIAL MOVEMENTS IN PATIENTS WITH PARKINSON'S DISEASE
511 Citations1987R. Benecke, John C. Rothwell +3 more
The problems exhibited by patients with Parkinson's disease when they try to perform two rapid sequential movements can be seen as a deficit in the capacity to switch from one motor program to another within an overall motor plan.
Journal of NeuroscienceTransition of Brain Activation from Frontal to Parietal Areas in Visuomotor Sequence Learning
478 Citations1998Katsuyuki Sakai, Okihide Hikosaka +4 more
The results suggest that the acquisition of visuomotor sequence learning requires frontal activation, whereas the retrieval of visUomotor sequences requires parietal activation, which might reflect the transition from the declarative stage to the procedural stage.
BrainFunctional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements
467 Citations1998Christian Gerloff
It is suggested that important aspects of information processing in the human motor system could be based on network-like oscillatory cortical activity and might be modulated on at least two levels, which to some extent can operate independently from each other: regional activation (task-related power) and inter-regional functional coupling.
Archives of General PsychiatryCerebral Glucose Metabolism in Childhood-Onset Obsessive-Compulsive Disorder
418 Citations1992Susan E. Swedo
Positron emission tomography revealed a significant decrease in normalized orbitofrontal regional cerebral glucose metabolism (relative to global metabolism) bilaterally among the treated patients, and the decrease was directly correlated with two measures of OCD improvement.
NeuroImageThe Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study
415 Citations1998Ivan Toni, Michael Krams +2 more
Experimental Brain ResearchDifferential roles of monkey striatum in learning of sequential hand movement
378 Citations1997S. Miyachi, Okihide Hikosaka +3 more
The results suggest that the anterior and posterior portions of the striatum participate in different aspects of learning of sequential movements.
Seminars in NeuroscienceFunctions of dopamine in the dorsal and ventral striatum
352 Citations1992Trevor W. Robbins, Barry J. Everitt
Manipulations of dopamine levels in the dorsal and ventral striatum are shown to affect the activation of behaviour in distinct, yet parallel ways, which depend upon the nature of the neocortical and limbic input to these structures.
Progress in NeurobiologyThe psychology of perseverative and stereotyped behaviour
292 Citations1994R.M. Ridley
Many forms of psychopathology in higher animals and humans include the production of maladaptive, repetitive behaviour which is both repetitive and excessive in amount whereas behaviour which represents a restriction of behavioural possibilities without excessive production can be described as perseverative.
Methods for NEURAL ENSEMBLE RECORDINGS
286 Citations1998Miguel A. L. Nicolelis
Methods for Neural Ensemble Recordings explores methods for using electrophysiological techniques for monitoring the concurrent activity of ensembles of single neurons and examines the many possible applications for this revolutionary method.
Journal of NeurophysiologyNeuronal Activity in Medial Frontal Cortex During Learning of Sequential Procedures
266 Citations1998Kae Nakamura, Katsuyuki Sakai +1 more
The results suggest that the pre-SMA, rather than SMA, is more involved in the acquisition of new sequential procedures.
Journal of NeurophysiologyModifications of Reward Expectation-Related Neuronal Activity During Learning in Primate Striatum
262 Citations1998Léon Tremblay, Jeffrey R. Hollerman +1 more
Investigating neuronal activity in the anterior striatum while monkeys repeatedly learned to associate new instruction stimuli with known behavioral reactions and reinforcers showed changes related to adaptations or reductions of expectations in new task situations and displayed activations that might serve to induce structural changes during learning.
Behavioural Brain ResearchResponses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus
257 Citations1983Edmund T. Rolls, Simon J. Thorpe +1 more
It is suggested that the anterior neostriatum contains neuronal mechanisms which are important in the process by which environmental cues are used in the preparation of behavioral responses, and in the initiation of particular behavioral responses made in particular situations to particular environmental stimuli.
Current Opinion in NeurobiologyPlasticity of adult sensorimotor representations
222 Citations1995John P. Donoghue
Of particular relevance to plasticity of cerebral cortical sensorimotor representations is recent evidence for the participation of intracortical horizontal pathways.
Current Opinion in NeurobiologyMnemonic functions of the basal ganglia
205 Citations1997Norman M. White
Evidence at several levels of analysis implicate dopamine release from nigro-striatal neurons in the reinforcement, or strengthening, of neural representations in the basal ganglia.
The Journal of Comparative NeurologyRepresentation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat
192 Citations1991Regina M. Carelli, Mark O. West
Neurons related to individual body parts were recorded throughout the entire anterior‐posterior extent of the dorsolateral striatum and representations of the head and face were located ventral to those of the limbs, despite substantial overlap in their overall distributions.
Archives of Neurology And PsychiatryCONTROL OF TWO SIMULTANEOUS VOLUNTARY MOTOR ACTS IN NORMALS AND IN PARKINSONISM
188 Citations1954Robert S. Schwab
In 50 patients with Parkinsonism, visual-motor reaction time tests have been routinely performed, and the values are close to normal in mild and moderately severe cases.
Current Opinion in NeurobiologyNeurobiology of skill and habit learning
187 Citations1995David P. Salmon, Nelson Butters
Recent evidence indicates that the basal ganglia are critical brain structures for motor-skill and habit learning, and may be important for the acquisition of some perceptual and cognitive skills.
Experimental Brain ResearchChanges in motor cortical activity during visuomotor adaptation
185 Citations1998S.P. Wise, Sohie Lee Moody +2 more
Data support the prediction that changes in task-related neuronal activity can be observed in M1 during motor adaptation, but fail to support the hypothesis that M1 and PMdc differ in this regard.
Journal of NeurophysiologyA region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements
167 Citations1990Mark O. West, Regina M. Carelli +5 more
Results show that functional representations of individual limbs can be demonstrated in the lateral striatum of the rat, within a subregion containing terminals of projections from somatic sensorimotor cortex.
Journal of NeuroscienceLoss of Lever Press-Related Firing of Rat Striatal Forelimb Neurons after Repeated Sessions in a Lever Pressing Task
113 Citations1997Regina M. Carelli, Martin Wolske +1 more
The change in firing suggests that the striatal activity present in early sessions may be necessary for the acquisition of, but not the automatic performance of, learned motor responses.
Annual Review of NeuroscienceTHE SIGNIFICANCE OF NEURAL ENSEMBLE CODES DURING BEHAVIOR AND COGNITION
85 Citations1997Sam A. Deadwyler, Robert E. Hampson
This review examines recent studies employing simultaneous recording of ten or more individual neurons in the mammalian brain and discusses whether ensemble information content reconstructed from single-neuron recordings may be underestimated if compared to ensembles where those same neurons were recorded simultaneously.
Journal of NeurophysiologyInfluence of Spatial Information on Responses of Tonically Active Neurons in the Monkey Striatum
64 Citations2006Sabrina Ravel, Pierangelo Sardo +2 more
Activity of tonically active neurons in the striatum of monkeys trained to make spatially directed movements elicited by visual stimuli presented ipsilaterally or contralaterally to the moving arm is examined to demonstrate that TANs are not limited to motivational processing, but may play a role in the processing of spatial attributes of stimulus and/or movement as well.
Journal of NeurophysiologyInfluence of Predictive Information on Responses of Tonically Active Neurons in the Monkey Striatum
62 Citations1998Paul Apicella, Sabrina Ravel +2 more
Responses of tonic striatal neurons to a trigger stimulus for movement were influenced by predictive information, suggesting an increased ability to predict the trigger onset during cued trials compared with uncued trials.
Journal of NeurophysiologyActivation on the Medial Wall During Remembered Sequences of Reaching Movements in Monkeys
61 Citations1997Nathalie Picard, Peter L. Strick
The findings suggest that the CMAd is involved more than any other medial area in the preparation for and/or execution of highly practiced, remembered sequences of movements.