The dynamics of dopamine in control of motor behavior (original) (raw)
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Dopamine Modulation in a Basal Ganglio-Cortical Network Implements Saliency-Based Gating of
Dopamine exerts two classes of effect on the sustained neural activity in prefrontal cortex that underlies working memory. Direct release in the cortex increases the contrast of prefrontal neurons, enhancing the robustness of storage. Release of dopamine in the striatum is associated with salient stimuli and makes medium spiny neurons bistable; this modulation of the output of spiny neurons affects prefrontal cortex so as to indirectly gate access to working memory and additionally damp sensitivity to noise. Existing models have treated dopamine in one or other structure, or have addressed basal ganglia gating of working memory exclusive of dopamine effects. In this paper we combine these mechanisms and explore their joint effect. We model a memory-guided saccade task to illustrate how dopamine's actions lead to working memory that is selective for salient input and has increased robustness to distraction.
Encoding by response duration in the basal ganglia
Journal of …, 2008
Several models have suggested that information transmission in the basal ganglia (BG) involves gating mechanisms, where neuronal activity modulates the extent of gate aperture and its duration. Here, we demonstrate that BG response duration is informative about a highly abstract stimulus feature and show that the duration of "gate opening" can indeed be used for information transmission through the BG. We analyzed recordings from three BG locations: the external part of the globus pallidus (GPe), the substantia nigra pars reticulata (SNr), and dopaminergic neurons from the substantia nigra pars compacta (SNc) during performance of a probabilistic visuomotor task. Most (Ͼ85%) of the neurons showed significant rate modulation following the appearance of cues predicting future reward. Trial-to-trial mutual information analysis revealed that response duration encoded reward prospects in many (42%) of the responsive SNr neurons, as well as in the SNc (26.9%), and the GPe (29.3%). Whereas the low-frequency discharge SNc neurons responded with only an increase in firing rate, SNr and GPe neurons with high-frequency tonic discharge responded with both increases and decreases. Conversely, many duration-informative neurons in SNr (68%) and GPe (50%) responded with a decreased rather than an increased rate. The response duration was more informative than the extreme (minimal or maximal) amplitude or spike count in responsive bins of duration-informative neurons. Thus response duration is not simply correlated with the discharge rate and can provide additional information to the target structures of the BG.
European Journal of Neuroscience, 2008
Here we challenge the view that reward-guided learning is solely controlled by the mesoaccumbens pathway arising from dopaminergic neurons in the ventral tegmental area and projecting to the nucleus accumbens. This widely accepted view assumes that reward is a monolithic concept, but recent work has suggested otherwise. It now appears that, in reward-guided learning, the functions of ventral and dorsal striata, and the cortico-basal ganglia circuitry associated with them, can be dissociated. Whereas the nucleus accumbens is necessary for the acquisition and expression of certain appetitive Pavlovian responses and contributes to the motivational control of instrumental performance, the dorsal striatum is necessary for the acquisition and expression of instrumental actions. Such findings suggest the existence of multiple independent yet interacting functional systems that are implemented in iterating and hierarchically organized cortico-basal ganglia networks engaged in appetitive behaviors ranging from Pavlovian approach responses to goal-directed instrumental actions controlled by action-outcome contingencies.
Frontiers in neural circuits, 2016
The brain enables animals to behaviorally adapt in order to survive in a complex and dynamic environment, but how reward-oriented behaviors are achieved and computed by its underlying neural circuitry is an open question. To address this concern, we have developed a spiking model of the basal ganglia (BG) that learns to dis-inhibit the action leading to a reward despite ongoing changes in the reward schedule. The architecture of the network features the two pathways commonly described in BG, the direct (denoted D1) and the indirect (denoted D2) pathway, as well as a loop involving striatum and the dopaminergic system. The activity of these dopaminergic neurons conveys the reward prediction error (RPE), which determines the magnitude of synaptic plasticity within the different pathways. All plastic connections implement a versatile four-factor learning rule derived from Bayesian inference that depends upon pre- and post-synaptic activity, receptor type, and dopamine level. Synaptic w...
Synchronization of Midbrain Dopaminergic Neurons Is Enhanced by Rewarding Events
Neuron, 2009
The basal ganglia network is divided into two functionally related subsystems: the neuromodulators and the main axis. It is assumed that neuromodulators adjust cortico-striatal coupling. This adjustment might depend on the response properties and temporal interactions between neuromodulators. We studied functional interactions between simultaneously recorded pairs of neurons in the basal ganglia while monkeys performed a classical conditioning task that included rewarding, neutral, and aversive events. Neurons that belong to a single neuromodulator group exhibited similar average responses, whereas main axis neurons responded in a highly diverse manner. Dopaminergic neuromodulators transiently increased trial-to-trial (noise) correlation following rewarding but not aversive events, whereas cholinergic neurons of the striatum decreased their trial-to-trial correlation. These changes in functional connectivity occurred at different epochs of the trial. Thus, the coding scheme of neuromodulators (but not main axis neurons) can be viewed as a singledimensional code that is further enriched by dynamic neuronal interactions. Neuron Basal Ganglia Correlations 696 Neuron 62, 695-704, June 11, 2009 ª2009 Elsevier Inc.
Assessing Selectivity in the Basal Ganglia: The “Gearbox” Hypothesis
Despite experimental evidence, the literature so far contains no systematic attempt to address the impact of cortical oscillations on the ability of the basal ganglia (BG) to select. In this study, we employed a state-of-the-art spiking neural model of the BG circuitry and investigated the effectiveness of this circuitry as an action selection device. We found that cortical frequency, phase, dopamine and the examined time scale, all have a very important impact on this process. Our simulations resulted in a canonical profile of selectivity, termed selectivity portraits, which suggests that the cortex is the structure that determines whether selection will be performed in the BG and what strategy will be utilized. Some frequency ranges promote the exploitation of highly salient actions, others promote the exploration of alternative options, while the remaining frequencies halt the selection process. Based on this behaviour, we propose that the BG circuitry can be viewed as the “gearb...
Is the short-latency dopamine response too short to signal reward error
Trends in Neurosciences, 1999
Unexpected stimuli which are behaviourally significant have the capacity to evoke a short latency, short duration burst of firing in mesencephalic dopamine neurones. An influential interpretation of the experimental data characterising this response proposes that dopamine neurones play a critical role in reinforcement learning by signalling errors in the prediction of future reward. In the present viewpoint we propose a different functional role for the short latency dopamine response in the mechanisms of associative learning.
The Enigmatic “Indirect Pathway” of the Basal Ganglia: A New Role
Neuron, 2018
Goal-directed behavior is processed in the dorsomedial striatum. Using a probabilistic reward paradigm, Nonomura et al. (2018) show that indirect pathway neurons signal when an action is incorrect and it is time to switch strategies, while the direct pathway remains active with a correct action.
Dopamine modulation in the basal ganglia locks the gate to working memory
Journal of Computational Neuroscience, 2006
The prefrontal cortex and basal ganglia are deeply implicated in working memory. Both structures are subject to dopaminergic neuromodulation in a way that exerts a critical influence on the proper operation of working memory. We present a novel network model to elucidate the role of phasic dopamine in the interaction of these two structures in initiating and maintaining mnemonic activity. We argue that neuromodulation plays a critical role in protecting memories against both internal and external sources of noise. Increases in cortical gain engendered by prefrontal dopamine release help make memories robust against external distraction, but do not offer protection against internal noise accompanying recurrent cortical activity. Rather, the output of the basal ganglia provides the gating function of stabilization against noise and distraction by enhancing select memories through targeted disinhibition of cortex. Dopamine in the basal ganglia effectively locks this gate by influencing the stability of Action editor: up and down states in the striatum. Dopamine's involvement in affective processing endows this gating with specificity to motivational salience. We model a spatial working memory task and show that these combined effects of dopamine lead to superior performance.