Motor learning transiently changes cortical somatotopy

Molina-Luna, Katiuska; Hertler, Benjamin; Buitrago, Manuel M.; Luft, Andreas R.

doi:10.1016/j.neuroimage.2007.11.018

Cited by 111 publications

(107 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The primary motor cortex (M1) is involved in the acquisition of novel movement sequences and skills (Nudo et al, 1996;Kleim et al, 1998;Luft et al, 2004;Molina-Luna et al, 2008). M1 harbors dopaminergic terminals (for review, see Luft and Schwarz, 2009) that optimize motor skill learning and the ability of M1 synapses to undergo long-term potentiation (LTP)-LTP is a cellular mechanism that is used in M1 during skill acquisition (RioultPedotti et al, 2000(RioultPedotti et al, , 2007.…”

Section: Introductionmentioning

confidence: 99%

Dopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning

Hosp¹,

Pekanovic²,

et al. 2011

View full text Add to dashboard Cite

The primary motor cortex (M1) of the rat contains dopaminergic terminals. The origin of this dopaminergic projection and its functional role for movement are obscure. Other areas of cortex receive dopaminergic projections from the ventral tegmental area (VTA) of the midbrain, and these projections are involved in learning phenomena. We therefore hypothesized that M1 receives a dopaminergic projection from VTA and that this projection mediates the learning of a motor skill by inducing cellular plasticity events in M1. Retrograde tracing from M1 of Long-Evans rats in conjunction with tyrosine hydroxylase immunohistochemistry identified dopaminergic cell bodies in VTA. Electrical stimulation of VTA induced expression of the immediate-early gene c-fos in M1, which was blocked by intracortical injections of D 1 and D 2 antagonists. Destroying VTA dopaminergic neurons prevented the improvements in forelimb reaching seen in controls during daily training. Learning recovered on administration of levodopa into the M1 of VTA-lesioned animals. Lesioning VTA did not affect performance of an already learned skill, hence, left movement execution intact. These findings provide evidence that dopaminergic terminals in M1 originate in VTA, contribute to M1 plasticity, and are necessary for successful motor skill learning. Because VTA dopaminergic neurons are known to signal rewards, the VTA-to-M1 projection is a candidate for relaying reward information that could directly support the encoding of a motor skill within M1.

show abstract

Section: Introductionmentioning

confidence: 99%

Dopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning

Hosp¹,

Pekanovic²,

et al. 2011

View full text Add to dashboard Cite

show abstract

“…With respect to spine formation and the size of the forelimb representations in M1, a return to baseline was observed one week after the training ended [5,12]. Thus, in comparison with synapses and motor maps, the plastic modifications of dendritic morphology follow a slower timecourse.…”

Section: Discussionmentioning

confidence: 96%

“…Behavioral tasks were performed as previously described [12]. The training cage was a 15 x 40 cm chamber (height 30 cm) with a vertical window (1 cm wide, 5 cm high, lower edge 2 cm above ground) in the front wall and a small light sensor in the rear wall (7 cm above ground).…”

Section: Experimental Setup and Behavioral Experimentsmentioning

confidence: 99%

“…An initial increase in spine formation for example is followed by an enhanced turnover that reduces the number of spines to baseline levels [5]. Whereas this concept of biphasic reorganization has been well demonstrated for spines [5], synaptic weights [11] and motor maps [12] it is unknown whether learning-induced growth of dendritic fields [4,13,14] is a lasting phenomenon or if a pruning occurs after a delay. To address this question, we measured dendritic morphology of layer V motoneurons at different time-points (day 0, day 30 and day 60) following acquisition of a skilled reaching task in rats.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Biphasic plasticity of dendritic fields in layer V motor neurons in response to motor learning

Gloor

Luft

Hosp

2015

Neurobiology of Learning and Memory

View full text Add to dashboard Cite

Motor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that advances through stages. An initial increment in spine formation is followed by pruning and maturation one week after training ended. A similar biphasic course was described for the size of the forelimb representation in M1. This study investigates the evolution of the dendritic architecture in response to motor skill training using Golgy-Cox silver impregnation in rat M1. After learning of a unilateral forelimb-reaching task to plateau performance, an increase in dendritic length of layer V pyramidal neurons (i.e. motor neurons) was observed that peaked one month after training ended. This increment in dendritic length reflected an expansion of the distal dendritic compartment. After one month dendritic arborization shrinks even though animals retain task performance. This pattern of evolution was observed for apical and basal dendrites alike -although the increase in dendritic length occurs faster in basal than in apical dendrites. Dendritic plasticity in response to motor training follows a biphasic course with initial expansion and subsequent shrinkage. This evolution takes fourth as long as the biphasic reorganization of spines or motor representations. AbstractMotor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that advances through stages. Dendritic spines grow initially followed by pruning and maturation approximately one week after training ended. A similar biphasic course was described for the size of the forelimb representation in M1. This study investigates the evolution of the dendritic architecture in response to motor skill training using Golgy-Cox silver impregnation in rat M1. After learning of a unilateral forelimb-reaching task to plateau performance, an increase in dendritic length of layer V pyramidal neurons (i.e. motor neurons) was observed that peaked one month after training ended. This increment in dendritic length reflected an expansion of the distal dendritic compartment. After one month dendritic arborization shrinks even though animals retain task performance. This pattern of evolution was observed for apical and basal dendrites alike -although the increase in dendritic length occurs faster in basal than in apical dendrites. Dendritic plasticity in response to motor training follows a biphasic course with initial expansion and subsequent shrinkage. This evolution takes fourth as long as the biphasic reorganization of spines or motor representations.3

show abstract

“…This phenomenon can be observed in rodents, primates, and humans (Kleim, Barbay, and Nudo, 1998;Nudo, Milliken, Jenkins, and Merzenich, 1996;Pascual-Leone, Nguyet, Cohen, Brasil-Neto, Cammarota, and Hallett, 1995). This enlargement is learning specific as it does not occur in response to mere motor activation and its magnitude is proportional to learning success (Kleim, Hogg, VandenBerg, Cooper, Bruneau, and Remple, 2004;Molina-Luna, Hertler, Buitrago, and Luft, 2008).…”

Section: Introductionmentioning

confidence: 88%

Temporal course of gene expression during motor memory formation in primary motor cortex of rats

Hertler

Buitrago

Luft

et al. 2016

Neurobiology of Learning and Memory

View full text Add to dashboard Cite

Motor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that depends on changes in gene expression. Here, we investigate the temporal profile of these changes during motor memory formation in response to a skilled reaching task in rats. mRNA-levels were measured 1h, 7h and 24h after the end of a training session using microarray technique. To assure learning specificity, trained animals were compared to a control group. In response to motor learning, genes are sequentially regulated with high time-point specificity and a shift from initial suppression to later activation. The majority of regulated genes can be linked to learning-related plasticity. In the gene-expression cascade following motor learning, three different steps can be defined: (1) an initial suppression of genes influencing gene transcription. (2) Expression of genes that support translation of mRNA in defined compartments. (3) Expression of genes that immediately mediates plastic changes. Gene expression peaks after 24h -this is a much slower time-course when compared to hippocampusdependent learning, where peaks of gene-expression can be observed 6-12h after training ended. AbstractMotor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that depends on changes in gene expression. Here, we investigate the temporal profile of these changes during motor memory formation in response to a skilled reaching task in rats. mRNA-levels were measured 1h, 7h and 24h after the end of a training session using microarray technique. To assure learning specificity, trained animals were compared to a control group. In response to motor learning, genes are sequentially regulated with high time-point specificity and a shift from initial suppression to later activation. The majority of regulated genes can be linked to learning-related plasticity. In the gene-expression cascade following motor learning, three different steps can be defined: 1) an initial suppression of genes influencing gene transcription. 2) Expression of genes that support translation of mRNA in defined compartments. 3) Expression of genes that immediately mediates plastic changes. Gene expression peaks after 24 hours -this is a much slower time-course when compared to hippocampus-dependent learning, where peaks of geneexpression can be observed 6 to 12 hours after training ended.3

show abstract

Motor learning transiently changes cortical somatotopy

Cited by 111 publications

References 24 publications

Dopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning

Dopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning

Biphasic plasticity of dendritic fields in layer V motor neurons in response to motor learning

Temporal course of gene expression during motor memory formation in primary motor cortex of rats

Contact Info

Product

Resources

About