Expanding the role of striatal cholinergic interneurons and the midbrain dopamine system in appetitive instrumental conditioning

The basal ganglia are a collection of subcortical nuclei thought to underlie a wide variety of vertebrate behavior. Although a great deal is known about the functional and physiological properties of the basal ganglia, relatively few models have been formally developed that have been tested against both behavioral and physiological data. Our previous work (Ashby FG, Crossley MJ. J Cogn Neurosci 23: 1549–1566, 2011) showed that a model grounded in the neurobiology of the basal ganglia could account for basic single-neuron recording data, as well as behavioral phenomena such as fast reacquisition that constrain models of conditioning. In this article we show that this same model accounts for a variety of appetitive instrumental conditioning phenomena, including the partial reinforcement extinction (PRE) effect, rapid and slowed reacquisition following extinction, and renewal of previously extinguished instrumental responses by environmental context cues.

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Subthalamic, not striatal, activity correlates with basal ganglia downstream activity in normal and parkinsonian monkeys

eLife ◽

10.7554/elife.16443 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 45

Author(s):

Marc Deffains ◽

Liliya Iskhakova ◽

Shiran Katabi ◽

Suzanne N Haber ◽

Zvi Israel ◽

...

Keyword(s):

Basal Ganglia ◽

Field Potential ◽

Temporal Discounting ◽

Projection Neurons ◽

Invasive Treatment ◽

Cholinergic Interneurons ◽

Striatal Projection Neurons ◽

Local Field Potential Lfp ◽

Spiking Activity

The striatum and the subthalamic nucleus (STN) constitute the input stage of the basal ganglia (BG) network and together innervate BG downstream structures using GABA and glutamate, respectively. Comparison of the neuronal activity in BG input and downstream structures reveals that subthalamic, not striatal, activity fluctuations correlate with modulations in the increase/decrease discharge balance of BG downstream neurons during temporal discounting classical condition task. After induction of parkinsonism with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), abnormal low beta (8-15 Hz) spiking and local field potential (LFP) oscillations resonate across the BG network. Nevertheless, LFP beta oscillations entrain spiking activity of STN, striatal cholinergic interneurons and BG downstream structures, but do not entrain spiking activity of striatal projection neurons. Our results highlight the pivotal role of STN divergent projections in BG physiology and pathophysiology and may explain why STN is such an effective site for invasive treatment of advanced Parkinson's disease and other BG-related disorders.

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The Basal Ganglia in Action

The Neuroscientist ◽

10.1177/1073858416654115 ◽

2016 ◽

Vol 23 (3) ◽

pp. 299-313 ◽

Cited By ~ 25

Author(s):

Henry H. Yin

Keyword(s):

Basal Ganglia ◽

Control Systems ◽

Position Control ◽

Brain Disorders ◽

Transition Control ◽

Feedback Control Systems ◽

Subcortical Nuclei ◽

Negative Feedback Control ◽

The Brain

The basal ganglia (BG) are the major subcortical nuclei in the brain. Disorders implicating the BG are characterized by diverse symptoms, but it remains unclear what these symptoms have in common or how they can be explained by changes in the BG circuits. This review summarizes recent findings that not only question traditional assumptions about the role of the BG in movement but also elucidate general computations performed by these circuits. To explain these findings, a new conceptual framework is introduced for understanding the role of the BG in behavior. According to this framework, the cortico-BG networks implement transition control in an extended hierarchy of closed loop negative feedback control systems. The transition control model provides a solution to the posture/movement problem, by postulating that BG outputs send descending signals to alter the reference states of downstream position control systems for orientation and body configuration. It also explains major neurological symptoms associated with BG pathology as a result of changes in system parameters such as multiplicative gain and damping.

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Basal Ganglia Paths Support Acute vs. Learned Execution, Not Movement vs. Stopping

10.20944/preprints201808.0157.v1 ◽

2018 ◽

Author(s):

Ari Rappoport

Keyword(s):

Basal Ganglia ◽

Receptor Expression ◽

Central Component ◽

Direct Path ◽

Standard Account ◽

Cholinergic Interneurons ◽

Neuroscience Research ◽

Indirect Path ◽

The Brain

The basal ganglia (BG) are a central component of the brain, crucial to the initiation, execution and learning of adaptive actions. The BG are the major site of the action of dopamine. An important aspect of the BG architecture is the existence of two paths, direct and indirect, having different projection targets and dopamine receptor expression. To understand the BG, dopamine, and related disorders, it is imperative to understand the two paths. The standard account used in neuroscience research for decades posits that the direct path supports movements, while the indirect path suppresses unselected or completed movements. This account is contradicted by converging evidence. Here, we explain why the arguments supporting the standard account are flawed, and present a new account, in which the role of the indirect path is completely opposite: to support learned execution. During acute events, ongoing execution is stopped, and the direct path allows coarse responses. These are refined by competition, and the resulting focused response is executed and learned by the indirect path, assisted by cholinergic interneurons. The new account allows a novel understanding of the symptoms of Parkinson's disease, and of its treatment by deep brain stimulation of the subthalamic nucleus.

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A Biologically Inspired Computational Model of Basal Ganglia in Action Selection

Computational Intelligence and Neuroscience ◽

10.1155/2015/187417 ◽

2015 ◽

Vol 2015 ◽

pp. 1-24 ◽

Cited By ~ 10

Author(s):

Chiara Baston ◽

Mauro Ursino

Keyword(s):

Basal Ganglia ◽

Previous History ◽

Action Selection ◽

Dopamine Depletion ◽

Behavioral Experiments ◽

Biologically Inspired ◽

Cholinergic Interneurons ◽

Hebb Rule ◽

History Of

The basal ganglia (BG) are a subcortical structure implicated in action selection. The aim of this work is to present a new cognitive neuroscience model of the BG, which aspires to represent a parsimonious balance between simplicity and completeness. The model includes the 3 main pathways operating in the BG circuitry, that is, the direct (Go), indirect (NoGo), and hyperdirect pathways. The main original aspects, compared with previous models, are the use of a two-term Hebb rule to train synapses in the striatum, based exclusively on neuronal activity changes caused by dopamine peaks or dips, and the role of the cholinergic interneurons (affected by dopamine themselves) during learning. Some examples are displayed, concerning a few paradigmatic cases: action selection in basal conditions, action selection in the presence of a strong conflict (where the role of the hyperdirect pathway emerges), synapse changes induced by phasic dopamine, and learning new actions based on a previous history of rewards and punishments. Finally, some simulations show model working in conditions of altered dopamine levels, to illustrate pathological cases (dopamine depletion in parkinsonian subjects or dopamine hypermedication). Due to its parsimonious approach, the model may represent a straightforward tool to analyze BG functionality in behavioral experiments.

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The Role of the Basal Ganglia in Somatosensory-Motor Interactions: Evidence from Neurophysiology and Behavior

10.3389/978-2-88963-475-0 ◽

2020 ◽

Keyword(s):

Basal Ganglia ◽

And Behavior

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Expression of FoxP2 in the basal ganglia regulates vocal motor sequences in the adult songbird

Nature Communications ◽

10.1038/s41467-021-22918-2 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Lei Xiao ◽

Devin P. Merullo ◽

Therese M. I. Koch ◽

Mou Cao ◽

Marissa Co ◽

...

Keyword(s):

Transcription Factor ◽

Basal Ganglia ◽

Dopamine Receptor ◽

Speech Disorders ◽

Receptor Expression ◽

Vocal Development ◽

Motor Actions

AbstractDisruption of the transcription factor FoxP2, which is enriched in the basal ganglia, impairs vocal development in humans and songbirds. The basal ganglia are important for the selection and sequencing of motor actions, but the circuit mechanisms governing accurate sequencing of learned vocalizations are unknown. Here, we show that expression of FoxP2 in the basal ganglia is vital for the fluent initiation and termination of birdsong, as well as the maintenance of song syllable sequencing in adulthood. Knockdown of FoxP2 imbalances dopamine receptor expression across striatal direct-like and indirect-like pathways, suggesting a role of dopaminergic signaling in regulating vocal motor sequencing. Confirming this prediction, we show that phasic dopamine activation, and not inhibition, during singing drives repetition of song syllables, thus also impairing fluent initiation and termination of birdsong. These findings demonstrate discrete circuit origins for the dysfluent repetition of vocal elements in songbirds, with implications for speech disorders.

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Adaptive Integration in the Visual Cortex by Depressing Recurrent Cortical Circuits

Neural Computation ◽

10.1162/neco.2008.06-07-546 ◽

2008 ◽

Vol 20 (7) ◽

pp. 1847-1872 ◽

Cited By ~ 24

Author(s):

Mark C. W. van Rossum ◽

Matthijs A. A. van der Meer ◽

Dengke Xiao ◽

Mike W. Oram

Keyword(s):

Visual Cortex ◽

Physiological Data ◽

High Contrast ◽

Cortical Circuits ◽

Response Latencies ◽

Low Contrast ◽

Visual Areas ◽

Higher Visual Areas ◽

Recurrent Connections

Neurons in the visual cortex receive a large amount of input from recurrent connections, yet the functional role of these connections remains unclear. Here we explore networks with strong recurrence in a computational model and show that short-term depression of the synapses in the recurrent loops implements an adaptive filter. This allows the visual system to respond reliably to deteriorated stimuli yet quickly to high-quality stimuli. For low-contrast stimuli, the model predicts long response latencies, whereas latencies are short for high-contrast stimuli. This is consistent with physiological data showing that in higher visual areas, latencies can increase more than 100 ms at low contrast compared to high contrast. Moreover, when presented with briefly flashed stimuli, the model predicts stereotypical responses that outlast the stimulus, again consistent with physiological findings. The adaptive properties of the model suggest that the abundant recurrent connections found in visual cortex serve to adapt the network's time constant in accordance with the stimulus and normalizes neuronal signals such that processing is as fast as possible while maintaining reliability.

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Possible cues driving context-specific adaptation of optocollic reflex in pigeons (Columba livia)

Journal of Neurophysiology ◽

10.1152/jn.00684.2011 ◽

2012 ◽

Vol 107 (2) ◽

pp. 704-717 ◽

Cited By ~ 1

Author(s):

Henri Gioanni ◽

Pierre-Paul Vidal

Keyword(s):

Columba Livia ◽

Motor Command ◽

Slow Phase ◽

Gaze Stabilization ◽

Specific Adaptation ◽

Body Vibration ◽

Fast Phase ◽

Context Specific ◽

Context Cues

Context-specific adaptation (Shelhamer M, Clendaniel R. Neurosci Lett 332: 200–204, 2002) explains that reflexive responses can be maintained with different “calibrations” for different situations (contexts). Which context cues are crucial and how they combine to evoke context-specific adaptation is not fully understood. Gaze stabilization in birds is a nice model with which to tackle that question. Previous data showed that when pigeons ( Columba livia) were hung in a harness and subjected to a frontal airstream provoking a flying posture (“flying condition”), the working range of the optokinetic head response [optocollic reflex (OCR)] extended toward higher velocities compared with the “resting condition.” The present study was aimed at identifying which context cues are instrumental in recalibrating the OCR. We investigated that question by using vibrating stimuli delivered during the OCR provoked by rotating the visual surroundings at different velocities. The OCR gain increase and the boost of the fast phase velocity observed during the “flying condition” were mimicked by body vibration. On the other hand, the newly emerged relationship between the fast-phase and slow-phase velocities in the “flying condition” was mimicked by head vibration. Spinal cord lesion at the lumbosacral level decreased the effects of body vibration, whereas lesions of the lumbosacral apparatus had no effect. Our data suggest a major role of muscular proprioception in the context-specific adaptation of the stabilizing behavior, while the vestibular system could contribute to the context-specific adaptation of the orienting behavior. Participation of an efferent copy of the motor command driving the flight cannot be excluded.

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