Effect of the Nigrostriatal Dopamine System on Acquired Neural Responses in the Striatum of Behaving Monkeys

Aosaki, Toshihiko; Graybiel, Ann M.; Kimura, Minoru

doi:10.1126/science.8023166

Cited by 379 publications

(337 citation statements)

References 26 publications

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“…There were also dynamic signal changes in the amygdala and the orbitomedial frontal cortex (OMFC), which are known to be involved in reward-based learning (35,36). Our results are thus consistent with models of basal ganglia function that propose that basal ganglia neurons integrate cortical signals with reward error signals carried by dopamine neurons during learning to build learned behaviors (26,27,37).…”

Section: Discussionsupporting

confidence: 77%

“…Similarly, recordings studies in the monkey's striatum showed that the associative and sensorimotor regions of the striatum contribute preferentially to the early and late stages of procedural learning, respectively (25). In rats, widely distributed changes in neuronal activity patterns have also been observed in the sensorimotor striatum during the course of learning (26,27), suggesting that the long-term representation of actions is built up through dynamic reorganization of neuronal activity in this territory. Finally, previous studies in humans have also reported activations within the associative striatum during the early stage of motor sequence learning (2,3,19).…”

Section: Discussionmentioning

confidence: 99%

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Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Lehericy

Benali

Moortele

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

548

449

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In this study, we used functional MRI (fMRI) at high field (3T) to track the time course of activation in the entire basal ganglia circuitry, as well as other motor-related structures, during the explicit learning of a sequence of finger movements over a month of training. Fourteen right-handed healthy volunteers had to practice 15 min daily a sequence of eight moves using the left hand. MRI sessions were performed on days 1, 14 and 28. In both putamen, activation decreased with practice in rostrodorsal (associative) regions. In contrast, there was a significant signal increase in more caudoventral (sensorimotor) regions of the putamen. Subsequent correlation analyses between signal variations and behavioral variables showed that the error rate (movement accuracy) was positively correlated with signal changes in areas activated during early learning, whereas reaction time (movement speed) was negatively correlated with signal changes in areas activated during advanced learning stages, including the sensorimotor putamen and globus pallidus. These results suggest the possibility that motor representations shift from the associative to the sensorimotor territories of the striato-pallidal complex during the explicit learning of motor sequences, suggesting that motor skills are stored in the sensorimotor territory of the basal ganglia that supports a speedy performance.functional MRI ͉ human ͉ subthalamic nucleus T here is now ample evidence from a number of sources that indicates that the basal ganglia are implicated in the formation of motor skills (1). In human studies using brain-imaging techniques, for example, changes of activity have been observed in the basal ganglia at different stages of the acquisition of motor abilities. Decreases of activity in the basal ganglia were reported during the early phase of trial-and-error learning of sequential movements (2). Using a similar task, Toni et al. (3) also reported a decrease of activity in the caudate nucleus, pre-supplementary motor area (SMA), and prefrontal cortex during the first hour of the acquisition process (3). By contrast, studies of implicit motor learning showed that the striatum was more active when subjects reached asymptotic performance, thus suggesting that this structure may be critical for the long-term storage of motor sequences (4-7). However, other investigations (8, 9) failed to document the presence of a greater increase in activity during the execution of well-learned sequential movements compared with the early learning phase.Although still conjectural, differences in the patterns of activation described above may reflect the involvement of different cortico-basal ganglia circuits during the acquisition process, because it is now known that cortical areas project to the striatum in separate associative, premotor, and sensorimotor circuits (10, 11). Indeed, previous imaging works have shown that rostral striatal areas are activated during learning of new motor sequences (2, 3) whereas the execution of well learned sequential movements invo...

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Lehericy

Benali

Moortele

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

548

449

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“…In addition, the firing rate change of cholinergic interneurons is not closely related to the execution of tasks, but rather to the presentation of the conditioned, trigger stimulus (Aosaki et al, 1995). However, the firing is not simply sensory in nature because the cholinergic interneurons acquire their responses during conditioning, and their responses undergo extinction along with the conditioned movement (Aosaki et al, 1994a(Aosaki et al, , 1994b. Thus, the cholinergic pause develops with the behavioral conditioning, and becomes linked to the conditioned stimulus that predicts reward.…”

Section: Different In Vivo Responses Of Spiny and Cholinergic Neuronsmentioning

confidence: 99%

“…The pause responses of the cholinergic neurons to conditioned trigger stimuli in learned movement tasks is abolished when dopaminergic inputs to the striatum are removed or are blocked by DA antagonists (Aosaki et al, 1994a(Aosaki et al, , 1994bWatanabe and Kimura, 1998). In DA-denervated animals, the firing patterns of cholinergic neurons are severely altered such that the neurons fire synchronized rhythmic bursts (Raz et al, 1996).…”

Section: Neurophysiological Influences Over the Firing Of Cholinergicmentioning

confidence: 99%

Cholinergic interneuron characteristics and nicotinic properties in the striatum

2002

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ABSTRACT:The neostriatum (dorsal striatum) is composed of the caudate and putamen. The ventral striatum is the ventral conjunction of the caudate and putamen that merges into and includes the nucleus accumbens and striatal portions of the olfactory tubercle. About 2% of the striatal neurons are cholinergic. Most cholinergic neurons in the central nervous system make diffuse projections that sparsely innervate relatively broad areas. In the striatum, however, the cholinergic neurons are interneurons that provide very dense local innervation. The cholinergic interneurons provide an ongoing acetylcholine (ACh) signal by firing action potentials tonically at about 5 Hz. A high concentration of acetylcholinesterase in the striatum rapidly terminates the ACh signal, and thereby minimizes desensitization of nicotinic acetylcholine receptors. Among the many muscarinic and nicotinic striatal mechanisms, the ongoing nicotinic activity potently enhances dopamine release. This process is among those in the striatum that link the two extensive and dense local arbors of the cholinergic interneurons and dopaminergic afferent fibers. During a conditioned motor task, cholinergic interneurons respond with a pause in their tonic firing. It is reasonable to hypothesize that this pause in the cholinergic activity alters action potential dependent dopamine release. The correlated response of these two broad and dense neurotransmitter systems helps to coordinate the output of the striatum, and is likely to be an important process in sensorimotor planning and learning.

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“…DA depletion within the dorsal striatum, for example, reduces the responsiveness of striatal neurons to auditory, visual and tactile stimuli [6,98,101,122]. Prior to DA depletion, approximately 22% of neurons sampled from the dorsolateral caudate of the cat responded to tactile stimulation of the face; only 6% showed such tactile responses after MPTP-induced DA depletion [101].…”

Section: Da Activity Gates the Throughput Of Sensorimotor And Incentimentioning

confidence: 99%

Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum

Horvitz

2002

Behavioural Brain Research

187

148

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Effect of the Nigrostriatal Dopamine System on Acquired Neural Responses in the Striatum of Behaving Monkeys

Cited by 379 publications

References 26 publications

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Cholinergic interneuron characteristics and nicotinic properties in the striatum

Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum

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