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Paralimbic system and striatum are involved in motivational behavior

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Abstract

Goal-directed rewarded behavior and goal-directed non-rewarded behavior are concerned with motivation. However, the neural substrates involved in goal-directed non-rewarded behaviors are unknown. Using functional magnetic resonance imaging, we investigated the brain activities of healthy individuals during a novel tool use (turning a screwdriver) to elucidate the relationship between the brain mechanism relevant to goal-directed non-rewarded behavior and motivation. We found that our designed behavioral task evoked activities in the orbitofrontal cortex, striatum, anterior insula, lateral prefrontal cortex, and anterior cingulate cortex compared with a meaningless task. These results suggest that activation in these cerebral regions play important roles in motivational behavior without tangible rewards.

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... Sensation, a ention, conscious processing, and memory are all highly selective as the behavioral systems direct social information processing 5 . Because of its central role in reinforcement, the mesolimbic reward circuit, together with the social behavioral network (paralimbic system) (Kiehl, 2006;Nishimura, Yoshii, Watanabe, & Ishiuchi, 2009;O'Connell & Hofmann, 2011b), functions as the "comparator" for social behavioral systems as these integrate sensory input and motor output (Depue & Collins, 1999). Dopamine (DA) has the general function of facilitating neural processes subserving motivation (Depue & Morrone-Strupinsky, 2005). ...
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The orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odours is represented. The orbitofrontal cortex also receives information about the sight of objects from the temporal lobe cortical visual areas, and neurons in it learn and reverse the visual stimulus to which they respond when the association of the visual stimulus with a primary reinforcing stimulus (such as taste) is reversed. This is an example of stimulus-reinforcement association learning, and is a type of stimulus-stimulus association learning. More generally, the stimulus might be a visual or olfactory stimulus, and the primary (unlearned) positive or negative reinforcer a taste or touch. A somatosensory input is revealed by neurons that respond to the texture of food in the mouth, including a population that responds to the mouth feel of fat. In complementary neuroimaging studies in humans, it is being found that areas of the orbitofrontal cortex are activated by pleasant touch, by painful touch, by taste, by smell, and by more abstract reinforcers such as winning or losing money. Damage to the orbitofrontal cortex can impair the learning and reversal of stimulus-reinforcement associations, and thus the correction of behavioural responses when there are no longer appropriate because previous reinforcement contingencies change. The information which reaches the orbitofrontal cortex for these functions includes information about faces, and damage to the orbitofrontal cortex can impair face (and voice) expression identification. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behavior, and thus in emotion. The approach described here is aimed at providing a fundamental understanding of how the orbitofrontal cortex actually functions, and thus in how it is involved in motivational behavior such as feeding and drinking, in emotional behavior, and in social behavior.
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The author proposes a general model of human motivation as a separate function at the interface between emotion and action, which can be ascribed to subcortical circuits that are mainly centered on a subset of the basal ganglia and on their limbic connections. It is argued that the long-standing historical understatement of the notion of motivation in neurology is not only due to the complexity of the issue, which has proven hard to disentangle from other domains of dysfunction, but also to the persistence of some misleading conceptual orientations in the way neurologists have considered the brain mechanisms of goal-directed action, torn between a nonspecific "activation" view and an exclusively cognitive conception of motivation. How combining early clinical intuitions of some psychiatrists, careful clinical observations of neurological patients, and data derived from experimental studies in animals provide the basis for a coherent model of human motivation and its specific impairment in clinical neurology is explained. Clinical implications that can be drawn from such a model for some neuropsychiatric conditions are proposed.
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We used functional magnetic resonance imaging to investigate brain activity related to motivational function of informative feedback stimuli in a time estimation task. In that task, subjects pressed a button as a response 3 s after a cue stimulus; a visual feedback stimulus was presented 2 s after the response. In a true feedback condition, subjects received true information (informative feedback) about their time-estimation performance. In the false feedback condition, the same visual signs were used, but they were presented randomly. Therefore, they were not related to actual performance. In the 20 subjects examined, higher hemodynamic responses were identified in the insular cortex, the thalamus, and the striatum by comparing the true feedback condition to the false feedback condition. The time estimation performance and subjective score on motivation were also markedly higher in the true feedback condition. The anterior insular cortex and striatal regions are known to be involved in motivational and reward processing. Therefore, the hemodynamic responses observed in this study suggest that the motivational function of the feedback information is a crucial factor for behavioral learning; it is considered that the informative feedback might serve as an implicit reward for humans.
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We examined neural basis underlying tool-use behavior to discuss whether or not the usage of a well-learned tool has a specific route. Regional cerebral blood flow was measured in healthy Japanese subjects using functional magnetic resonance imaging (fMRI) during object pick-up using chopsticks, object pick-up using the hand, pantomiming the use of chopsticks, imagining the use of chopsticks, and imagining the use of the hand. First, the left inferior parietal lobule (IPL) was found to selectively contribute to tasks requiring explicit retrieval of tool-related hand movements that were pantomiming task and imagery task. This finding provides supporting evidence for the ideomotor apraxia (IMA) model proposed by Buxbaum (2001). However, departing from Buxbaum's (2001) proposal, the actual use of a well-learned tool displays distinct processing routes to those for pantomime and imagining. A comparison of these tasks revealed that activation in the lateral part of the right cerebellum increased during execution of tool-use, and this activity was considered to reflect the internal model for tools proposed by Imamizu et al. (2000, 2003).
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The orbitofrontal cortex (OFC) is important in motivation and emotion. We previously reported reward expectancy-related delay activities during a delayed reaction time task in primate OFC neurons. To further investigate the significance of the OFC in motivational operations, we examined pre-instruction, baseline activities of OFC neurons in relation to reward expectancy during the delayed reaction time task. In this task, an instruction cue indicated whether reward would be present or absent in the trial. Each set of four consecutive trials constituted one block within which three different kinds of rewards and one trial with no reward were given in a fixed order that differed from the monkey's reward preference. We identified two types of OFC neurons with reward expectancy-related pre-instruction activities: Step-type neurons showed stepwise changes (increase or decrease) in pre-instruction activity toward the trial with a particular outcome, which usually was the most or least attractive within a block; Pref-type neurons showed pre-instruction activity changes according to the monkey's preference for each trial's outcome. We propose that Step-type and Pref-type neurons are related to long-range and short-range reward expectancies of a particular outcome, respectively. The OFC is considered to play important roles in goal-directed behaviour by adjusting the motivational level toward a certain (current or future) outcome of a particular motivational significance based on the two kinds of reward expectancy processes. Impairments in goal-directed behaviour by OFC patients may be caused by a lack of long-range expectancy or by a deficit in compromising between short-range and long-range expectancies.
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Despite an increasing focus on the neural basis of human decision making in neuroscience, relatively little attention has been paid to decision making in social settings. Moreover, although human social decision making has been explored in a social psychology context, few neural explanations for the observed findings have been considered. To bridge this gap and improve models of human social decision making, we investigated whether acquiring a good reputation, which is an important incentive in human social behaviors, activates the same reward circuitry as monetary rewards. In total, 19 subjects participated in functional magnetic resonance imaging (fMRI) experiments involving monetary and social rewards. The acquisition of one's good reputation robustly activated reward-related brain areas, notably the striatum, and these overlapped with the areas activated by monetary rewards. Our findings support the idea of a "common neural currency" for rewards and represent an important first step toward a neural explanation for complex human social behaviors.
Regulation of firing of dopaminergic neurons and control of goal-directed behaviors
  • Grace