A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input

Gale, Samuel D.; Person, Abigail L.; Perkel, David J.

doi:10.1002/cne.21700

Cited by 91 publications

(123 citation statements)

References 82 publications

(101 reference statements)

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“…In mammals, a similar rule has been found to describe synaptic connections from cortex to the basal ganglia (37). Thus, a causal inverse may reside in the efferent synapses of a cortical area upstream of the basal ganglia homolog; or, based on anatomy, a causal inverse could be connected to a dopaminergic ventral tegmental area (38,39), thereby establishing a possible link of our findings with reinforcement learning theories (see below). Other candidate pathways for the causal inverse could lead to LMAN through HVC or through the thalamo-cortical projections from the dorsolateral nucleus of the thalamus (DLM).…”

Section: Discussionsupporting

confidence: 75%

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: Discussionsupporting

confidence: 75%

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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“…The projection from Area X to the VP is formed from collaterals of thalamus-projecting pallidal-like neurons (Gale et al, 2008). In line with this finding, our bulk tracer injections into both the MSt and Area X revealed axon branching suggestive of collateral terminals in the VP (Fig.…”

Section: Medial Basal Ganglia Structures: Mst Area X and Vpsupporting

confidence: 62%

“…Area X is known to project to the thalamic nucleus DLM (Bottjer et al, 1989) and the VP (Gale et al, 2008). To compare the output of Area X directly with those of the MSt and other basal ganglia structures, we began by injecting the bidirectional tracer Alexa-conjugated 10K dextran amine into both Area X and MSt of male zebra finches.…”

Section: Medial Basal Ganglia Structures: Mst Area X and Vpmentioning

confidence: 99%

Organization of the songbird basal ganglia, including area X

Person

Gale

Farries

et al. 2008

J of Comparative Neurology

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131

160

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Area X is a songbird basal ganglia nucleus that is required for vocal learning. Both Area X and its immediate surround, the medial striatum (MSt), contain cells displaying either striatal or pallidal characteristics. We used pathway-tracing techniques to compare directly the targets of Area X and MSt with those of the lateral striatum (LSt) and globus pallidus (GP). We found that the zebra finch LSt projects to the GP, substantia nigra pars reticulata (SNr) and pars compacta (SNc), but not the thalamus. The GP is reciprocally connected with the subthalamic nucleus (STN) and projects to the SNr and motor thalamus analog, the ventral intermediate area (VIA). In contrast to the LSt, Area X and surrounding MSt project to the ventral pallidum (VP) and dorsal thalamus via pallidal-like neurons. A dorsal strip of the MSt contains spiny neurons that project to the VP. The MSt, but not Area X, projects to the ventral tegmental area (VTA) and SNc, but neither MSt nor Area X projects to the SNr. Largely distinct populations of SNc and VTA dopaminergic neurons innervate Area X and surrounding the MSt. Finally, we provide evidence consistent with an indirect pathway from the cerebellum to the basal ganglia, including Area X. Area X projections thus differ from those of the GP and LSt, but are similar to those of the MSt. These data clarify the relationships among different portions of the oscine basal ganglia as well as among the basal ganglia of birds and mammals.

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“…During development, the avian VP also expresses Dlx2, Nkx2.1, yet no Pax6, similar to the situation in the mammalian VP (Puelles et al, 2000). Functionally, the VP constitutes an integral link between the dopaminergic reward system and song nuclei (Gale et al, 2008). The dopaminergic reinforcement of a bird's own song involves the disinhibition of the dopaminergic neurons by inhibition of VP, suggesting that the reward system and song nuclei compose a functional pathway for vocal learning and reinforcement of song production (Gale and Perkel, 2010).…”

Section: Birdsmentioning

confidence: 83%

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

O’Connell

Hofmann

2011

J of Comparative Neurology

822

841

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All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation. J. Comp. Neurol. 519:3599-3639, 2011. INDEXING TERMS: social behavior; comparative neuroanatomy; amphibian; reptile; bird; teleost; reward system; social behavior network; limbic system; neural circuitsThroughout their lives, all animals constantly face situations that provide either challenges (e.g., aggression, predation) or opportunities (e.g., reproduction, foraging, habitat selection) (for a detailed review, see O'Connell and Hofmann, 2011). In all cases, environmental cues are processed by sensory systems into a meaningful biological signal while internal physiological cues (e.g., condition, maturity) and prior experience are integrated at the same time. This process usually results in behavioral actions that are adaptive, i.e., beneficial to the animal. To accomplish this, an animal's nervous system must evaluate the salience of a stimulus and elicit a context-appropriate behavioral response. Despite tremendous progress in understanding the ecology and evolution of social behavior (Lorenz, 1952;Tinbergen, 1963;Lehrman, 1965;von Frisch, 1967;Krebs and Davies, 1993;Stephens, 2008), it is less understood where in the brain these decisions (e.g., about mate choice or territory defense) are made and how these brain circuits have arisen over the course of vertebrate evolution.Recent research has begun to decipher the neural basis of social decision-making. In mammals in particular, the neural circuits that evaluate stimulus salience and/or regulate social behavior have been uncovered to some degree: the mesolimbic reward system and social behavior network (Fig. 1). It is becoming increasingly clear that the reward system (including but not limited to the midbrain dopaminergic system) is the neural circuit where the salience of an external stimulus is evaluated (Deco and Rolls, 2005;Wickens et al., 2007), as appetitive beh...

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A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input

Cited by 91 publications

References 82 publications

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

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

Organization of the songbird basal ganglia, including area X

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

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