Covert skill learning in a cortical-basal ganglia circuit

Charlesworth, Jonathan D.; Warren, Timothy L.; Brainard, Michael S.

doi:10.1038/nature11078

Cited by 114 publications

(112 citation statements)

References 25 publications

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“…That is, the causal inverse could be formed when young birds engage in motor explorations during the sensorimotor learning phase, in agreement with LMAN's known role in producing song variability in this critical phase (41,42). Once the inverse mapping is established, it could be used to select downstream motor patterns in agreement with a sensory target and therefore steer the developing song in the right direction.…”

Section: Discussionmentioning

confidence: 64%

“…A promising avenue into LMAN-mediated fast learning are recent experiments on negative song reinforcement in which LMAN, after having been transiently prevented from contributing to vocal output, was shown after recovery to instantaneously mediate vocal escape behaviors (41), which was suggested to provide support for a motor efference copy to LMAN (41). Alternatively, we propose that such instantaneous escape behaviors arise from a causal inverse model upstream of LMAN.…”

Section: Discussionmentioning

confidence: 97%

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Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

Giret

Kornfeld²,

Ganguli

et al. 2014

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

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Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.lateral magnocellular nucleus of the anterior nidopallium | Hebbian learning | mirror neuron

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Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 97%

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

Giret

Kornfeld²,

Ganguli

et al. 2014

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

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“…First, LMAN bursting may be especially effective at modulating activity in the song motor nucleus RA, driving fluctuations in song that could function as motor exploration (24-27, 36, 45-47). Second, given recent evidence that LMAN can adaptively bias song output (16,48,49), it is also possible that song-locked bursting contributes to song plasticity directly, by instructing specific changes in the synaptic connections between the premotor nucleus HVC and RA via spike-timing-dependent mechanisms (24,27,36,47,50,51). Third, burst firing might also increase the synchrony of activity across multiple neurons in LMAN, and thus enhance their effectiveness in influencing RA and subsequent song output.…”

Section: Discussionmentioning

confidence: 99%

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

Kojima

Kao

Doupe

2013

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

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Basal ganglia-thalamocortical circuits are critical for motor control and motor learning. Classically, basal ganglia nuclei are thought to regulate motor behavior by increasing or decreasing cortical firing rates, and basal ganglia diseases are assumed to reflect abnormal overall activity levels. More recent studies suggest instead that motor disorders derive from abnormal firing patterns, and have led to the hypothesis that surgical treatments, such as pallidotomy, act primarily by eliminating pathological firing patterns. Surprisingly little is known, however, about how the basal ganglia normally influence task-related cortical activity to regulate motor behavior, and how lesions of the basal ganglia influence cortical firing properties. Here, we investigated these questions in a songbird circuit that has striking homologies to mammalian basal ganglia-thalamocortical circuits but is specialized for singing. The “cortical” outflow nucleus of this circuit is required for song plasticity and normally exhibits increased firing during singing and song-locked burst firing. We found that lesions of the striato-pallidal nucleus in this circuit prevented hearing-dependent song changes. These basal ganglia lesions also stripped the cortical outflow neurons of their patterned burst firing during singing, without changing their spontaneous or singing-related firing rates. Taken together, these results suggest that the basal ganglia are essential not for normal cortical firing rates but for driving task-specific cortical firing patterns, including bursts. Moreover, such patterned bursting appears critical for motor plasticity. Our findings thus provide support for therapies that aim to treat basal ganglia movement disorders by normalizing firing patterns.

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“…attention) are closely engaged with the EMPS, error awareness increases. Furthermore, recent evidence shows the capacity of the basal ganglia (through the basal ganglia-cortical pathways) to implement successful performances that were initially produced by other brain regions, indicating precise functional connections between basal ganglia circuits and the motor regions that directly control performance (Charlesworth et al, 2012). Also, the basal ganglia generate a variety of behaviors during execution of task and learn to implement the successful behaviors in their repertoire to meet the target (Sur & Schultz 1999).…”

Section: Error Commission: Different Types One Sourcementioning

confidence: 99%