Schultz, Wolfram. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80: 1–27, 1998. The effects of lesions, receptor blocking, electrical self-stimulation, and drugs of abuse suggest t...

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Predictive Reward Signal of Dopamine Neurons

https://lsa.umich.edu/psych/research&labs/berridge/publications/Berridge&RobinsonBrResRev1998.pdf

What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?

The authors present a unified account of 2 neural systems concerned with the development and expression of adaptive behaviors: a mesencephalic dopamine system for reinforcement learning and a “generic” error-processing system associated with the anterior cingulate cortex The existence of the error-processing system has been inferred from the error-related negativity (ERN), a component of the event-related brain potential elicited when human participants commit errors in reaction-time tasks The authors propose that the ERN is generated when a negative reinforcement learning signal is conveyed to the anterior cingulate cortex via the mesencephalic dopamine system and that this signal is used by the anterior cingulate cortex to modify performance on the task at hand They provide support for this proposal using both computational modeling and psychophysiological experimentation

/pdf/the-neural-basis-of-human-error-processing-reinforcement-246y7vy4ka.pdf

The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity.

Drug addiction, dysregulation of reward, and allostasis.

The basal ganglia: focused selection and inhibition of competing motor programs.

The basal ganglia are neural structures within the motor and cognitive control circuits in the mammalian forebrain and are interconnected with the neocortex by multiple loops. Dysfunction in these parallel loops caused by damage to the striatum results in major defects in voluntary movement, exemplified in Parkinson's disease and Huntington's disease. These parallel loops have a distributed modular architecture resembling local expert architectures of computational learning models. During sensorimotor learning, such distributed networks may be coordinated by widely spaced striatal interneurons that acquire response properties on the basis of experienced reward.

https://science.sciencemag.org/content/sci/265/5180/1826.full.pdf

The basal ganglia and adaptive motor control

Dysfunction of the nigrostriatal dopamine system results in marked disorders of movement such as occur in Parkinson's disease. Functions of this dopamine-containing projection system were examined in monkeys trained in a classical conditioning task, and the effects of striatal dopamine depletion were tested. Unilateral dopamine loss substantially reduced the acquired sensory responsiveness of striatal neurons monitored electrophysiologically. This effect was ipsilateral and selective, and could be reversed by apomorphine. These results suggest that the primate nigrostriatal system modulates expression of neuronal response plasticity in the striatum during sensorimotor learning.

https://science.sciencemag.org/content/sci/265/5170/412.full.pdf

Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys

1. Tonically active neurons (TANs) in the primate striatum develop transient responses to sensory conditioning stimuli during behavioral training in classical conditioning tasks. In this study we examined the temporal characteristics of such TAN responses and mapped the sites of TANs responding to auditory and visual conditioned stimuli in the striatum in macaque monkeys. We further mapped the locations of TANs recorded acutely in the squirrel monkey striatum in relation to the neurochemically distinguished striosome and matrix compartments of the striatum, and made quantitative comparisons between the densities and compartmental distributions of TANs and those of four major types of striatal interneuron identified by histochemical and immunohistochemical staining. 2. We made recordings from 858 TANs at different sites in the striatum in two behaving macaque monkeys at different times during training with auditory (click) and visual (light-emitting diode flash) conditioning stimuli. TANs distributed across large parts of the striatum developed responses to the conditioning stimuli. The responses comprised a decrement of tonic firing (pause) followed by a rebound excitation. Measurements were made of the onsets, offsets, and durations of the pauses of individual TANs and of the interspike intervals (ISIs) of the same cells. 3. The mean duration of the pause responses (268.3 ms) was greater than the mean ISI of the same neurons (181 ms), suggesting that the pause represents an active suppression of TAN firing. The coefficient of variation (CV) for the pause responses was 0.28, compared with a CV of 0.63 for the same cells' ISIs. The population CV for the pauses was 0.16, compared with a population CV of 0.20 for the ISIs. These data, together with temporal analysis of the responses and population histograms, suggest that the pauses became temporally aligned across large parts of the striatum after learning. Analyses of variance (ANOVAs) were carried out to determine whether there were differences in the onset and offset latencies of the pause response or in the durations of the pause responses for TANs at different sites. These analyses suggested that, with rare exceptions, there was no difference in the timing of the TAN responses across large (> 10 mm3) parts of the striatum. 4. Comparisons of TAN responses in different regions of the striatum showed that, for responses to a given modality of conditioned stimulus, there were no significant differences in pause offset times for TANs recorded in the caudate nucleus or putamen, or for TANs recorded in more anterior or more posterior parts of these nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)

Temporal and spatial characteristics of tonically active neurons of the primate's striatum

The thalamus provides a massive input to the striatum, but despite accumulating evidence, the functions of this system remain unclear. It is known, however, that the centromedian (CM) and parafascicular (Pf) nuclei of the thalamus can strongly influence particular striatal neuron subtypes, notably including the cholinergic interneurons of the striatum (CINs), key regulators of striatal function. Here, we highlight the thalamostriatal system through the CM-Pf to striatal CINs. We consider how, by virtue of the direct synaptic connections of the CM and PF, their neural activity contributes to the activity of CINs and striatal projection neurons (SPNs). CM-Pf neurons are strongly activated at sudden changes in behavioral context, such as switches in action-outcome contingency or sequence of behavioral requirements, suggesting that their activity may represent change of context operationalized as associability. Striatal CINs, on the other hand, acquire and loose responses to external events associated with particular contexts. In light of this physiological evidence, we propose a hypothesis of the CM-Pf-CINs system, suggesting that it augments associative learning by generating an associability signal and promotes reinforcement learning guided by reward prediction error signals from dopamine-containing neurons. We discuss neuronal circuit and synaptic organizations based on in vivo/in vitro studies that we suppose to underlie our hypothesis. Possible implications of CM-Pf-CINs dysfunction (or degeneration) in brain diseases are also discussed by focusing on Parkinson's disease.

Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events

Toshihiko Aosaki

Papers

The basal ganglia and adaptive motor control

Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys

Temporal and spatial characteristics of tonically active neurons of the primate's striatum

Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events