The Sensorimotor Striatum Is Necessary for Serial Order Learning

Central to the production of adaptive behavior is the ability to learn the temporal order of behavioral elements (e.g., A, B, C). Yet little is known about neural substrates of serial order in self-initiated behavioral sequences. The present study assessed the contributions of specific dorsal striatal regions to the acquisition of serial order in mice, using a two-action sequence task without instructive cues. Excitotoxic lesions of the sensorimotor (dorsolateral) striatum dramatically impaired the acquisition of a simple sequence; in contrast, lesions of the associative (dorsomedial) striatum had no significant effect. Neither lesion caused gross motor impairments or affected the learning of nonsequential actions. These results demonstrate for the first time a critical role of the sensorimotor striatum in the learning of serial order.

• Publication year

  2010

• Venue

  Journal of Neuroscience

• Publication date

  2010-11-03

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1523/JNEUROSCI.3989-10.2010PMID 21048130PMCID PMC3181000
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The Role of the Murine Motor Cortex in Action Duration and Order

  2009influential reference
• Evidence of Action Sequence Chunking in Goal-Directed Instrumental Conditioning and Its Dependence on the Dorsomedial Prefrontal Cortex

  2009cited by this paper
• The Role of Striatum in Initiation and Execution of Learned Action Sequences in Rats

  2006cited by this paper
• Cortical control of motor sequences.

  2006cited by this paper
• Anticipatory activity in primary motor cortex codes memorized movement sequences.

  2005cited by this paper
• The role of the dorsomedial striatum in instrumental conditioning

  2005cited by this paper
• Blockade of NMDA receptors in the dorsomedial striatum prevents action–outcome learning in instrumental conditioning

  2005cited by this paper
• Contributions of striatal subregions to place and response learning.

  2004cited by this paper
• Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning

  2004cited by this paper
• The Basal Ganglia

  2004cited by this paper
• Cortex, striatum and cerebellum: control of serial order in a grooming sequence

  2004cited by this paper
• Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery

  2004cited by this paper
• Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex

  2004cited by this paper
• The mouse brain in stereotaxic coordinates

  2003cited by this paper
• The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry

  2002cited by this paper
• A neural correlate of oculomotor sequences in supplementary eye field.

  2002cited by this paper
• The prefrontal cortex--an update: time is of the essence.

  2001cited by this paper
• The prefrontal cortex—an update: Time of the essence

  2001cited by this paper
• Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis.

  1999cited by this paper
• Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements.

  1998cited by this paper
• Coding of Serial Order by Neostriatal Neurons: A “Natural Action” Approach to Movement Sequence

  1998cited by this paper
• The basal ganglia and chunking of action repertoires.

  1998cited by this paper
• Differential roles of monkey striatum in learning of sequential hand movement

  1997cited by this paper
• Motivational control of heterogeneous instrumental chains.

  1995cited by this paper
• The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats.

  1993cited by this paper
• Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations.

  1991cited by this paper
• A simple ordering of neocortical areas established by the compartmental organization of their striatal projections.

  1990cited by this paper
• The organization of the projection from the cerebral cortex to the striatum in the rat.

  1989cited by this paper
• The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain.

  1987cited by this paper
• Disturbance of sequential movements in patients with Parkinson's disease.

  1987cited by this paper
• Book reviewHandbook of Chemical Neuroanatomy: Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series).

  1986cited by this paper
• Dopamine depletion in a striatal subregion disrupts performance of a skilled motor task in the rat.

  1985cited by this paper
• Frontal lobes and the temporal organization of memory.

  1985cited by this paper
• Operant regulation of feeding: a static analysis.

  1983cited by this paper
• Evidence for a role of the caudate nucleus in the sequential organization of behavior.

  1982cited by this paper
• Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man.

  1982cited by this paper
• Higher Cortical Functions in Man

  1980cited by this paper
• The co-ordination and regulation of movements

  1967cited by this paper
• Cerebral mechanisms in behavior : the Hixon symposium

  1951cited by this paper

• The Secondary Motor Cortex Encodes Aversive Signals and Exerts an Inhibitory Control of Motor Sequence Learning in Mice

  2026cites this paper
• Refinement of efficient encodings of movement in the dorsolateral striatum throughout learning

  2025cites this paper
• Consolidation of a recurrent choice pattern into a fixed action schema requires the orbitofrontal cortex

  2025cites this paper
• Impairment of Group I Metabotropic Glutamate Receptors in the Dorsal Striatum of the R451C‐Neuroligin 3 Mouse Model of Autism Spectrum Disorder

  2025cites this paper
• Formation of an auditory sensory representation in posterior striatum emerges during a brief temporal window of associative learning in normal and hearing-impaired gerbils

  2025cites this paper
• Refinement of efficient encodings of movement in the dorsolateral striatum throughout learning

  2024cites this paper
• Adaptation of sequential action benefits from timing variability related to lateral basal ganglia circuitry

  2024cites this paper
• Parallel executive pallio‐motor loops in the pigeon brain

  2024cites this paper
• Harnessing early multimodal motor training to drive motor recovery and brain-wide structural reorganization after stroke

  2024cites this paper
• The NK1 antagonist L-733,060 facilitates sequence learning

  2023influential citation
• Corticostriatal dynamics underlying components of binge-like consumption of palatable food in mice.

  2023cites this paper
• Comparative Roles of the Caudate and Putamen in the Serial Order of Behavior: Effects of Striatal Glutamate Receptor Blockade on Variable versus Fixed Spatial Self-Ordered Sequencing in Marmosets

  2023cites this paper
• Visual Sequence Encoding is Enhanced by Predictable Music Pairing via Modulating Medial Temporal Lobe and Its Connectivity with Frontostriatal Loops

  2023cites this paper
• Role of the basal ganglia in innate and learned behavioural sequences

  2023cites this paper
• Multiple Memory Subsystems: Reconsidering Memory in the Mind and Brain

  2023cites this paper
• Nucleus accumbens and dorsal medial striatal dopamine and neural activity are essential for action sequence performance

  2023cites this paper
• The deep cerebellar nuclei to striatum disynaptic connection contributes to skilled forelimb movement.

  2023cites this paper
• Clinical neuroscience and neurotechnology: An amazing symbiosis

  2022cites this paper
• Dissociating the contributions of sensorimotor striatum to automatic and visually guided motor sequences

  2022cites this paper
• The Neural Basis of Behavioral Sequences in Cortical and Subcortical Circuits

  2022cites this paper
• Dynamic adaptation of sequential action benefits from cortico-basal ganglia-related temporal variability

  2022cites this paper
• Similar striatal activity exerts different control over automatic and flexible motor sequences

  2022cites this paper
• Action sequence dynamics rely on accessory hyperdirect pathway-related targets in the striatum

  2022cites this paper
• Blocking NK1 receptors disrupts the sequential and temporal organization of chain grooming in rats.

  2021cites this paper
• Opposing Roles of the Dorsolateral and Dorsomedial Striatum in the Acquisition of Skilled Action Sequencing in Rats

  2021cites this paper
• Nigrostriatal Dopamine Signals Sequence-Specific Action-Outcome Prediction Errors

  2021cites this paper
• The basal ganglia control the detailed kinematics of learned motor skills

  2021cites this paper
• Neuroplasticity induced by the retention period of a complex motor skill learning in rats.

  2021cites this paper
• Habit formation viewed as structural change in the behavioral network

  2021influential citation
• α-Synuclein Selectively Impairs Motor Sequence Learning and Value Sensitivity: Reversal by the Adenosine A2A Receptor Antagonists.

  2021cites this paper
• Corticostriatal dynamics underlying components of binge-like eating in mice

  2021cites this paper
• Interpreting the role of the striatum during multiple phases of motor learning

  2021cites this paper
• Endocannabinoids and Dopamine Balance Basal Ganglia Output

  2020cites this paper
• Gestational alcohol exposure disrupts cognitive function and striatal circuits in adult offspring

  2020cites this paper
• How the brain gets a roaring campfire

  2020cites this paper
• Optogenetic interrogation of the role of striatal patches in habit formation and inhibition of striatal dopamine

  2020cites this paper
• Inactivation of the Prelimbic Cortex Attenuates Operant Responding in Both Physical and Behavioral Contexts.

  2020cites this paper
• Striatal network modeling in Huntington’s Disease

  2020cites this paper
• Lesion of striatal patches disrupts habitual behaviors and increases behavioral variability

  2019cites this paper
• Physical and computational methods of investigating the relationship between stress, cognition, and behavior in the context of the KOR-dynorphin system

  2019cites this paper
• It takes two to tango: Dorsal direct and indirect pathways orchestration of motor learning and behavioral flexibility

  2019influential citation
• Exploring the relationship between actions, habits, and automaticity in an action sequence task

  2019cites this paper
• A neural network for uncertainty anticipation and information seeking

  2019cites this paper
• An open cortico-basal ganglia loop allows limbic control over motor output via the nigrothalamic pathway

  2019cites this paper
• Contributions of the basal ganglia to action sequence learning and performance.

  2019cites this paper
• Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

  2019influential citation
• The basal ganglia can control learned motor sequences independently of motor cortex

  2019cites this paper
• Chemogenetic inhibition in the dorsal striatum reveals regional specificity of direct and indirect pathway control of action sequencing

  2019influential citation
• Long‐term plasticity of glutamatergic input from the subthalamic nucleus to the entopeduncular nucleus

  2018cites this paper
• Neural basis of proximal influences on choice: recent reinforcement, inter-trial interval, and uncertainty

  2018cites this paper
• Recent Insights into Corticostriatal Circuit Mechanisms underlying Habits: Invited review for Current Opinions in Behavioral Sciences.

  2018cites this paper
• Motor improvement requires an increase in presynaptic protein expression and depends on exercise type and age

  2018cites this paper
• Alpha2-Containing Glycine Receptors Promote Neonatal Spontaneous Activity of Striatal Medium Spiny Neurons and Support Maturation of Glutamatergic Inputs

  2018cites this paper
• Lesions of ventrolateral striatum eliminate lose‐shift but not win‐stay behaviour in rats

  2018cites this paper
• Bidirectional Control of Reversal in a Dual Action Task by Direct and Indirect Pathway Activation in the Dorsolateral Striatum in Mice

  2017cites this paper
• Sensory Processing in the Dorsolateral Striatum: The Contribution of Thalamostriatal Pathways

  2017cites this paper
• Basal ganglia and autism – a translational perspective

  2017cites this paper
• Neurophysiology of rule switching in the corticostriatal circuit.

  2017cites this paper
• Treadmill Exercise Prevents Increase of Neuroinflammation Markers Involved in the Dopaminergic Damage of the 6-OHDA Parkinson’s Disease Model

  2017cites this paper
• Cortico‐striatal language pathways dynamically adjust for syntactic complexity: A computational study

  2017cites this paper
• Identifying motor functional neurological disorder using resting-state functional connectivity

  2017cites this paper
• Review of preclinical studies on pediatric general anesthesia-induced developmental neurotoxicity.

  2017cites this paper
• Single and repeated exposures to the volatile anesthetic isoflurane do not impair operant performance in aged rats.

  2016cites this paper
• Complementary Contributions of Striatal Projection Pathways to Action Initiation and Execution.

  2016cites this paper
• Distinct neuroplasticity processes are induced by different periods of acrobatic exercise training.

  2016cites this paper
• Procedural learning as a measure of functional impairment in a mouse model of ischemic stroke.

  2016cites this paper
• Dorsolateral neostriatum contribution to incentive salience: opioid or dopamine stimulation makes one reward cue more motivationally attractive than another

  2016cites this paper
• Striatal Circuits as a Common Node for Autism Pathophysiology

  2016cites this paper
• The role of opponent basal ganglia outputs in behavior

  2016cites this paper
• The Role of the Basal Ganglia in Executing and Learning Complex Motor Sequences

  2016cites this paper
• Rule Encoding in Orbitofrontal Cortex and Striatum Guides Selection

  2016cites this paper
• The Basal Ganglia and Hierarchical Control in Voluntary Behavior

  2016cites this paper
• Patterns of Modulation in the Activity and Connectivity of Motor Cortex during the Repeated Generation of Movement Sequences

  2015cites this paper
• Hierarchical control of goal-directed action in the cortical–basal ganglia network

  2015cites this paper
• Basal Ganglia Regulation of Motivated Behaviors

  2015cites this paper
• Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements

  2015cites this paper
• Different protocols of treadmill exercise induce distinct neuroplastic effects in rat brain motor areas.

  2015cites this paper
• Input- and Output-Specific Regulation of Serial Order Performance by Corticostriatal Circuits.

  2015influential citation
• Basal Ganglia Outputs Map Instantaneous Position Coordinates during Behavior

  2015cites this paper
• Distributed Patterns of Reactivation Predict Vividness of Recollection

  2015cites this paper
• Hierarchical models of goal-directed and automatic actions

  2015cites this paper
• Unraveling the neural circuitry of sequence-based navigation using a combined fos imaging and computational approach

  2014cites this paper
• Action, time and the basal ganglia

  2014cites this paper
• Striatal cholinergic interneuron regulation and circuit effects

  2014cites this paper
• Lesions of the dorsomedial striatum delay spatial learning and render cue-based navigation inflexible in a water maze task in mice

  2014cites this paper
• Is there a tape recorder in your head? How the brain stores and retrieves musical melodies

  2014influential citation
• Improved Executive Function and Callosal White Matter Microstructure after Rhythm Exercise in Huntington's Disease

  2014cites this paper
• Region‐specific impairments in striatal synaptic transmission and impaired instrumental learning in a mouse model of Angelman syndrome

  2014cites this paper
• Understanding the mechanisms of cognitive impairments in developmental coordination disorder

  2014cites this paper
• The role of the substantia nigra in posture control

  2014cites this paper
• The Representation of Order Information in Auditory-Verbal Short-Term Memory

  2014cites this paper
• Translational potential of the touchscreen-based methodology to assess cognitive abilities in mice

  2014cites this paper
• How Basal Ganglia Outputs Generate Behavior

  2014cites this paper
• Cortico-Basal Ganglia Networks and the Neural Substrates of Actions

  2014cites this paper
• Coding of sequential behaviors by anterior cingulate cortex ensembles

  2014cites this paper
• Striatal firing rate reflects head movement velocity

  2014cites this paper
• Mouse models of neurodevelopmental disease of the basal ganglia and associated circuits.

  2014influential citation
• Transient middle cerebral artery occlusion prevents habit formation in C57Bl/6J mice

  2013cites this paper
• Unilateral skill acquisition induces bilateral NMDA receptor subunit composition shifts in the rat sensorimotor striatum.

  2013cites this paper
• Striatum‐dependent habits are insensitive to both increases and decreases in reinforcer value in mice

  2013cites this paper