Masataka Watanabe

Tokyo Metropolitan Institute of Medical Science, Edo, Tōkyō, Japan

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Publications (19)90.01 Total impact

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    ABSTRACT: An optimal level of dopamine (DA) in the mammalian prefrontal cortex (PFC) is critical for higher cognitive control of behavior. Too much or too little DA in the PFC induces impairment in working memory (WM) task performance. PFC DA is also concerned with motivation. When reward is anticipated and/or delivered, an increase in PFC DA release is observed. In the primate, more preferred reward induces enhanced WM-related neuronal activity in the dorsolateral PFC (DLPFC). We hypothesized that there would be more DA release in the primate DLPFC when more preferred, as compared with less preferred, reward is delivered during a WM task. Contrary to our hypothesis, we found higher DA release in the DLPFC when less rather than more preferred reward was used during a WM task, while unpredictable free reward delivery induced an increase in DLPFC DA release irrespective of the difference in the incentive value of the reward. Behaviorally, the monkey was more motivated with preferred than with less preferred reward, although it performed the task almost without error irrespective of the difference in the reward. Considering that mild stress induces an increase in DA release in the mammalian PFC, performing a WM task for less preferred reward could have been mildly stressful, and this mild stress may have induced more DLPFC DA release in the present study. The higher DA release in the DLPFC with less preferred reward may be beneficial for monkeys to cope with mildly stressful and unfavorable situations to achieve proficient WM task performance.
    Behavioural brain research 02/2014; 266. DOI:10.1016/j.bbr.2014.02.009 · 3.39 Impact Factor
  • Takayuki Hosokawa, Masataka Watanabe
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    ABSTRACT: Humans and animals must work to support their survival and reproductive needs. Because resources are limited in the natural environment, competition is inevitable, and competing successfully is vitally important. However, the neuronal mechanisms of competitive behavior are poorly studied. We examined whether neurons in the lateral prefrontal cortex (LPFC) showed response sensitivity related to a competitive game. In this study, monkeys played a video shooting game, either competing with another monkey or the computer, or playing alone without a rival. Monkeys performed more quickly and more accurately in the competitive than in the noncompetitive games, indicating that they were more motivated in the competitive than in the noncompetitive games. LPFC neurons showed differential activity between the competitive and noncompetitive games showing winning- and losing-related activity. Furthermore, activities of prefrontal neurons differed depending on whether the competition was between monkeys or between the monkey and the computer. These results indicate that LPFC neurons may play an important role in monitoring the outcome of competition and enabling animals to adapt their behavior to increase their chances of obtaining a reward in a socially interactive environment.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 05/2012; 32(22):7662-71. DOI:10.1523/JNEUROSCI.6479-11.2012 · 6.75 Impact Factor
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    ABSTRACT: Human neuroimaging studies have demonstrated the presence of a "default system" in the brain, which shows a "default mode of brain activity," i.e., greater activity during the resting state than during an attention-demanding cognitive task. The default system mainly involves the medial prefrontal and medial parietal areas, including the anterior and posterior cingulate cortex. It has been proposed that this default activity is concerned with internal thought processes. Recently, it has been indicated that chimpanzees show high metabolic levels in these medial brain areas during rest. Correlated low-frequency spontaneous activity as measured by functional magnetic resonance imaging was observed between the medial parietal and medial prefrontal areas in the anesthetized monkey. However, there have been few attempts to demonstrate a default system that shows task-induced deactivation in nonhuman primates. We conducted a positron emission tomography study with [(15)O]H(2)O to demonstrate a default mode of brain activity in the awake monkey sitting on a primate chair. Macaque monkeys showed higher level of regional blood flow in these medial brain areas as well as lateral and orbital prefrontal areas during rest compared with that under a working memory task, suggesting the existence of internal thought processes in the monkey. However, during rest in the monkey, the highest level of blood flow relative to that in other brain regions was observed not in the default system but in the dorsal striatum, suggesting that regions with the highest cerebral blood flow during rest may differ depending on the resting condition and/or species.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 11/2009; 29(46):14463-71. DOI:10.1523/JNEUROSCI.1786-09.2009 · 6.75 Impact Factor
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    Masataka Watanabe, Masamichi Sakagami
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    ABSTRACT: The prefrontal cortex (PFC) appears to be important for processing both cognitive and motivational context information. Primate lateral PFC (LPFC) neurons are involved in cognitive context-dependent stimulus coding by responding differently to an identical stimulus according to the task situation. Such context-dependent LPFC activity appears to be supported by context-representing activity, observed also in LPFC neurons, in which the baseline activity differs as a function of the task. In LPFC, there are also neurons that code stimulus on the basis of motivational context. This motivational context is represented in differential baseline activity as a function of the reward context. In the orbitofrontal cortex (OFC), there are neurons that code stimuli depending on the motivational context as well as neurons that represent motivational context information. Furthermore, we found LPFC neurons that coded the stimulus depending on both the cognitive and motivational context, as well as LPFC neurons that represented both the cognitive and motivational context. For adaptive behavior, it is important to code the meaning of the environmental situation based on the context. While OFC is predominantly concerned with processing motivational context information, LPFC seems to play important roles in integrating the cognitive and motivational context for adaptive goal-directed behavior.
    Cerebral Cortex 10/2007; 17 Suppl 1:i101-9. DOI:10.1093/cercor/bhm067 · 8.31 Impact Factor
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    ABSTRACT: Economic theories of decision making are based on the principle of utility maximization, and reinforcement-learning theory provides computational algorithms that can be used to estimate the overall reward expected from alternative choices. These formal models not only account for a large range of behavioral observations in human and animal decision makers, but also provide useful tools for investigating the neural basis of decision making. Nevertheless, in reality, decision makers must combine different types of information about the costs and benefits associated with each available option, such as the quality and quantity of expected reward and required work. In this article, we put forward the hypothesis that different subdivisions of the primate frontal cortex may be specialized to focus on different aspects of dynamic decision-making processes. In this hypothesis, the lateral prefrontal cortex is primarily involved in maintaining the state representation necessary to identify optimal actions in a given environment. In contrast, the orbitofrontal cortex and the anterior cingulate cortex might be primarily involved in encoding and updating the utilities associated with different sensory stimuli and alternative actions, respectively. These cortical areas are also likely to contribute to decision making in a social context.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 09/2007; 27(31):8170-3. DOI:10.1523/JNEUROSCI.1561-07.2007 · 6.75 Impact Factor
  • Masamichi Sakagami, Masataka Watanabe
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    ABSTRACT: The prefrontal cortex (PFC), particularly the lateral prefrontal cortex (LPFC), has an important role in cognitive information processing. The area receives projections from sensory association cortices and sends outputs to motor-related areas. Neurons in LPFC code the behavioral significance of stimuli, which can be abstract precursors for complex motor commands and are structured hierarchically. Loss of these neurons leads to a lack of flexibility in decision making, such as seen in stereotyped behaviors. However, to make more appropriate decisions the code for behavioral significance has to reflect the subject's own desires and demands. Indeed, LPFC has connections with reward-related areas, such as the orbitofrontal cortex (OFC), basal ganglia, and medial prefrontal cortex. Recently, many studies have reported reward modulation of neural codes of behavioral significance. Using an asymmetric reward paradigm, we can investigate the functional specificity of LPFC neurons that code both cognitive information and motivational information. In this review, we will discuss details of neuronal properties of LPFC neurons from the viewpoints of cognitive information processing and motivational information processing, and the question of how these two pieces of information are integrated. Abstract coding and contextual representations in the cognitive information processing are functional characteristics of LPFC. Such functional specificity in LPFC cognitive processes is supported by a long-term scale of reward history in the motivational information processing. The integration enables us to make an elaborate decision with respect to goal-directed behavior in complex circumstances.
    Annals of the New York Academy of Sciences 06/2007; 1104:89-107. DOI:10.1196/annals.1390.010 · 4.31 Impact Factor
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    Masataka Watanabe
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    ABSTRACT: The lateral prefrontal cortex (LPFC), which is important for higher cognitive activity, is also concerned with motivational operations; this is exemplified by its activity in relation to expectancy of rewards. In the LPFC, motivational information is integrated with cognitive information, as demonstrated by the enhancement of working-memory-related activity by reward expectancy. Such activity would be expected to induce changes in attention and, subsequently, to modify behavioral performance. Recently, the effects of motivation and emotion on neural activities have been examined in several areas of the brain in relation to cognitive-task performance. Of these areas, the LPFC seems to have the most important role in adaptive goal-directed behavior, by sending top-down attention-control signals to other areas of the brain.
    Current Opinion in Neurobiology 05/2007; 17(2):213-9. DOI:10.1016/j.conb.2007.02.007 · 6.77 Impact Factor
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    ABSTRACT: Primate prefrontal delay neurons are involved in retaining task-relevant cognitive information in working memory (WM). Recent studies have also revealed primate prefrontal delay neurons that are related to reward/omission-of-reward expectancy. Such reward-related delay activities might constitute "affective WM" (Davidson, 2002). "Affective" and "cognitive" WM are both concerned with representing not what is currently being presented, but rather what was presented previously or might be presented in the future. However, according to the original and widely accepted definition, WM is the "temporary storage and manipulation of information for complex cognitive tasks". Reward/omission-of-reward expectancy-related neuronal activity is neither prerequisite nor essential for accurate task performance; thus, such activity is not considered to comprise the neural substrates of WM. Also, "affective WM" might not be an appropriate usage of the term "WM". We propose that WM- and reward/omission-of-reward expectancy-related neuronal activity are concerned with representing which response should be performed in order to attain a goal (reward) and the goal of the response, respectively. We further suggest that the prefrontal cortex (PFC) plays a crucial role in the integration of cognitive (for example, WM-related) and motivational (for example, reward expectancy-related) operations for goal-directed behaviour. The PFC could then send this integrated information to other brain areas to control the behaviour.
    Cortex 02/2007; 43(1):53-64. DOI:10.1016/S0010-9452(08)70445-3 · 6.04 Impact Factor
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    ABSTRACT: Both appetitive and aversive outcomes can reinforce animal behavior. It is not clear, however, whether the opposing kinds of reinforcers are processed by specific or common neural mechanisms. To investigate this issue, we studied macaque monkeys that performed a memory-guided saccade task for three different outcomes, namely delivery of liquid reward, avoidance of air puff, and feedback sound only. Animals performed the task best in rewarded trials, intermediately in aversive trials, and worst in sound-only trials. Most task-related activity in lateral prefrontal cortex was differentially influenced by the reinforcers. Aversive avoidance had clear effects on some prefrontal neurons, although the effects of rewards were more common. We also observed neurons modulated by both positive and negative reinforcers, reflecting reinforcement or attentional processes. Our results demonstrate that information about positive and negative reinforcers is processed differentially in prefrontal cortex, which could contribute to the role of this structure in goal-directed behavior.
    Neuron 10/2006; 51(6):861-70. DOI:10.1016/j.neuron.2006.08.031 · 15.98 Impact Factor
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    ABSTRACT: The lateral prefrontal cortex (LPFC) is important in cognitive control. During the delay period of a working memory (WM) task, primate LPFC neurons show sustained activity that is related to retaining task-relevant cognitive information in WM. However, it has not yet been determined whether LPFC delay neurons are concerned exclusively with the cognitive control of WM task performance. Recent studies have indicated that LPFC neurons also show reward and/or omission-of-reward expectancy-related delay activity, while the functional relationship between WM-related and reward/omission-of-reward expectancy-related delay activity remains unclear. To clarify the functional significance of LPFC delay-period activity for WM task performance, and particularly the functional relationship between these two types of activity, we examined individual delay neurons in the primate LPFC during spatial WM (delayed response) and non-WM (reward-no-reward delayed reaction) tasks. We found significant interactions between these two types of delay activity. The majority of the reward expectancy-related neurons and the minority of the omission-of-reward expectancy-related neurons were involved in spatial WM processes. Spatial WM-related neurons were more likely to be involved in reward expectancy than in omission-of-reward expectancy. In addition, LPFC delay neurons observed during the delayed response task were not concerned exclusively with the cognitive control of task performance; some were related to reward/omission-of-reward expectancy but not to WM, and many showed more memory-related activity for preferred rewards than for less-desirable rewards. Since employing a more preferred reward induced better task performance in the monkeys, as well as enhanced WM-related neuronal activity in the LPFC, the principal function of the LPFC appears to be the integration of cognitive and motivational operations in guiding the organism to obtain a reward more effectively.
    Experimental Brain Research 11/2005; 166(2):263-76. DOI:10.1007/s00221-005-2358-y · 2.17 Impact Factor
  • Kazuo Hikosaka, Masataka Watanabe
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    ABSTRACT: 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.
    European Journal of Neuroscience 03/2004; 19(4):1046-54. DOI:10.1111/j.0953-816X.2004.03120.x · 3.67 Impact Factor
  • Masataka Watanabe
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    ABSTRACT: The term “context” seems to be the key word for understanding the function of the prefrontal cortex (PFC). Primate lateral PFC (LPFC) neurons show activity changes depending on the cognitive context by responding differently to the identical stimulus according to the task requirement. LPFC neurons are also involved in monitoring the cognitive context by showing differential baseline activities depending on the task requirement.The LPFC plays important roles in motivational operations as well. We recently found primate LPFC neurons that appeared to represent the motivational context in a delayed reaction task.Representation of the cognitive context is to be used to suppress competing behaviors and to coordinate execution over temporally extended periods.Representation of the motivational context may be used to detect the congruency or discrepancy between expectancy and outcome and may serve for the acquisition/maintenance and modification of behavioral strategies. For goal-directed behavior, it is essential to integrate the cognitive and motivational information. Thus, the functional significance of the LPFC seems to lie in representing and integrating the cognitive and motivational context for goal-directed behavior.
    International Congress Series 10/2003; 1250:371-382. DOI:10.1016/S0531-5131(03)00189-4
  • Tohru Kodama, Kazuo Hikosaka, Masataka Watanabe
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    ABSTRACT: Glutamate is a major neurotransmitter in the mammalian brain and glutamatergic neurotransmission in the frontal cortex is indicated to play important roles in cognitive operations. We previously examined changes in extracellular dopamine in the primate frontal cortex in cognitive tasks, and in this paper we extend this to glutamate. We employed, as cognitive tasks, a delayed alternation task where the animal must retain information in working memory, and a sensory-guided task in which there is no working memory requirement but there may be more sensory processing requirements. Using the in vivo microdialysis method, we examined changes in extracellular glutamate concentration in the dorsolateral, arcuate, orbitofrontal, and premotor areas of the primate frontal cortex. Compared to basal rest levels, we observed significant increases in glutamate concentration in dorsolateral and arcuate areas of the prefrontal cortex during the sensory-guided task, but did not find significant changes in any of the frontal areas examined during the delayed alternation task. When glutamate concentration was compared between the delayed alternation and sensory-guided tasks, difference was observed only in the dorsolateral prefrontal cortex, especially in the ventral lip area of the principal sulcus. The results indicate the importance of glutamate in processing sensory information but not in retaining information in working memory in the primate dorsolateral and arcuate prefrontal cortex. We also compared the concentration of glutamate and dopamine in the tasks. We found a double dissociation in the concentration of glutamate and dopamine in the dorsolateral area: there was an increase in glutamate but no change in dopamine during the sensory-guided task, whereas there was an increase in dopamine but no change in glutamate during the delayed alternation task. It is thus suggested that in the primate dorsolateral prefrontal cortex, increased glutamate tone without dopamine increase facilitates sensory-guided task performance, while increased dopamine tone without glutamate increase is beneficial for working memory task performance.
    Experimental Brain Research 08/2002; 145(2):133-41. DOI:10.1007/s00221-002-1084-y · 2.17 Impact Factor
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    ABSTRACT: Attention is reported to be maintained by monoamines, acetylcholine and amino acids systems. Changes in the releases of these neurotransmitters during the three stages comprising quiet wake (QW) and two arousal states (AW), which are activated from different sources, were investigated. Norepinephrine releases during AW were significantly higher than that during QW. Conversely, the levels of acetylcholine and serotonin that were released did not change significantly among these three stages. The interesting observation was the dissociation of the increase between glutamate and dopamine releases in the two AW states. The results indicate that attention level is related to the amount of norepinephrine release, and that attention quality is related to the interaction between dopamine and glutamate releases.
    Psychiatry and Clinical Neurosciences 07/2002; 56(3):341-2. DOI:10.1046/j.1440-1819.2002.00977.x · 1.62 Impact Factor
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    ABSTRACT: The prefrontal cortex is involved in acquiring and maintaining information about context, including the set of task instructions and/or the outcome of previous stimulus-response sequences. Most studies on context-dependent processing in the prefrontal cortex have been concerned with such executive functions, but the prefrontal cortex is also involved in motivational operations. We thus wished to determine whether primate prefrontal neurons show evidence of representing the motivational context learned by the monkey. We trained monkeys in a delayed reaction task in which an instruction cue indicated the presence or absence of reward. In random alternation with no reward, the same one of several different kinds of food and liquid rewards was delivered repeatedly in a block of approximately 50 trials, so that reward information would define the motivational context. In response to an instruction cue indicating absence of reward, we found that neurons in the lateral prefrontal cortex not only predicted the absence of reward but also represented more specifically which kind of reward would be omitted in a given trial. These neurons seem to code contextual information concerning which kind of reward may be delivered in following trials. We also found prefrontal neurons that showed tonic baseline activity that may be related to monitoring such motivational context. The different types of neurons were distributed differently along the dorsoventral extent of the lateral prefrontal cortex. Such operations in the prefrontal cortex may be important for the monkey to maximize reward or to modify behavioral strategies and thus may contribute to executive control.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 04/2002; 22(6):2391-400. · 6.75 Impact Factor
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    ABSTRACT: Learning theory emphasizes the importance of expectations in the control of instrumental action. This study investigated the variation of behavioral reactions toward different rewards as an expression of differential expectations of outcomes in primates. We employed several versions of two basic behavioral paradigms, the spatial delayed response task and the delayed reaction task. These tasks are commonly used in neurobiological studies of working memory, movement preparation, and event expectation involving the frontal cortex and basal ganglia. An initial visual instruction stimulus indicated to the animal which one of several food or liquid rewards would be delivered after each correct behavioral response, or whether or not a reward could be obtained. We measured the reaction times of the operantly conditioned arm movement necessary for obtaining the reward, and the durations of anticipatory licking prior to liquid reward delivery as a Pavlovian conditioned response. The results showed that both measures varied depending on the reward predicted by the initial instruction. Arm movements were performed with significantly shorter reaction times for foods or liquids that were more preferred by the animal than for less preferred ones. Still larger differences were observed between rewarded and unrewarded trials. An interesting effect was found in unrewarded trials, in which reaction times were significantly shorter when a highly preferred reward was delivered in the alternative rewarded trials of the same trial block as compared to a less preferred reward. Anticipatory licks preceding the reward were significantly longer when highly preferred rather than less preferred rewards, or no rewards, were predicted. These results demonstrate that behavioral reactions preceding rewards may vary depending on the predicted future reward and suggest that monkeys differentially expect particular outcomes in the presently investigated tasks.
    Experimental Brain Research 11/2001; 140(4):511-8. DOI:10.1007/s002210100856 · 2.17 Impact Factor
  • Neuroscience Research 01/1998; 31. DOI:10.1016/S0168-0102(98)82343-2 · 2.15 Impact Factor
  • Tohru Kodama, Masataka Watanabe, Kazuo Hikosaka
    Neuroscience Research 01/1997; 28. DOI:10.1016/S0168-0102(97)90692-1 · 2.15 Impact Factor
  • Neuroscience Research 01/1996; 25. DOI:10.1016/0168-0102(96)89240-6 · 2.15 Impact Factor