Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill

By Henry H. Yin, S. Mulcare, Monica R. F. Hilário, E. Clouse, Terrell Holloway, M. I. Davis, A. Hansson, D. Lovinger, Rui M. Costa. Nature Neuroscience, 2009

793 citations recorded by the source corpus.

The learning of new skills is characterized by an initial phase of rapid improvement in performance and a phase of more gradual improvements as skills are automatized and performance asymptotes. Using in vivo striatal recordings, we observed region-specific changes in neural activity during the different phases of skill learning, with the associative or dorsomedial striatum being preferentially engaged early in training and the sensorimotor or dorsolateral striatum being engaged later in training. Ex vivo recordings from medium spiny striatal neurons in brain slices of trained mice revealed that the changes observed in vivo corresponded to regional- and training-specific changes in excitatory synaptic transmission in the striatum. Furthermore, the potentiation of glutamatergic transmission observed in dorsolateral striatum after extensive training was preferentially expressed in striatopallidal neurons, rather than striatonigral neurons. These findings demonstrate that region- and pathway-specific plasticity sculpts the circuits involved in the performance of the skill as it becomes automatized.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/77beaaf8a8fdda4f82c6bb5011826289f9312488

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In Cellular and Molecular Neuroscience

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Citations in the corpus

Goals and Habits in the Brain (2013, positive): “There is also explicit evidence for the transfer from dorsomedial to dorsolateral over the course of training (Belin et al., 2009; Graybiel, 2008; Yin et al., 2009; Thorn et al., 2010).”
The Neuroanatomical Organization of the Basal Ganglia (2010, background): “…striatum associative cortex loop plays an important role in the early phases of skill acquisition, whereas the dorsolateral striatum sensorimotor cortex loop is more involved once the skill has been established and the action program becomes more automated and inflexible (Yin et al., 2009).”
Neuroanatomical and Neurochemical Substrates of Timing (2011, background): “…timing may be considered a type of conditioned behavior that follows the rule of habit formation, which is a major component of addictive behavior (see Kalivas, 2008) and is also related to altered neural responses in the dorsal striatum (Takahashi et al, 2007; Yin et al, 2004, 2008, 2009).”
Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation (2015, neutral): “, the associative, prefrontal-connected portions) [3,12,60,62–68].”
Humanized Foxp2 accelerates learning by enhancing transitions from declarative to procedural performance (2014, background): “Proc Natl Acad Sci USA 95(21):12695–12700.”
A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors (2009, background): “The mechanisms by which basal ganglia circuitry support motor learning are largely unknown, but evidence suggests that the basal ganglia are necessary to express recently learned behavior (12), and that changes in neural activity in response to learning appear first in basal ganglia circuits (13, 14”
Neural reactivations during sleep determine network credit assignment (2017, methodology): “Analyses of neural firing variability and neuronal pair correlations—The modulation characteristics of each neuron in the BMI task in the two frames of reference (namely, ‘task-start’ and ‘task-end’) were examined using the following: (1) Fano factor, which is a statistical measure of the dynamics o”
Neuroplasticity subserving motor skill learning (2011, positive): “For example, in vivo recordings in behaving rodents revealed that the sensorimotor striatum is engaged later in training, when performance in an accelerated rotarod task asymptoted (Yin et al., 2009).”
Distinct coincidence detectors govern the corticostriatal spike timing‐dependent plasticity (2010, background): “…DOI: 10.1113/jphysiol.2010.188466 and memory (Martin et al. 2000; Martin & Morris, 2002; Lynch, 2004), the corticostriatal long-term plasticity provides a fundamental mechanism for the function of the basal ganglia in procedural learning (Di Filippo et al. 2009; Wickens, 2009; Yin et al. 2009).”
Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits (2015, positive): “…functionally distinguished by previous studies (Castañé et al., 2010; Faure et al., 2005; Featherstone and McDonald, 2004; Yin and Knowlton, 2004; Yin et al., 2004, 2005a, 2009, 2005b), leading us to hypothesize that SNc projections to these areas might also participate in separable circuits.”