Robust representation of stable object values in the oculomotor basal ganglia: Our gaze tends to be directed to objects previously associated with rewards. Such object values change flexibly or remain stable. Here we present evidence that the monkey substantia nigra pars reticulata (SNr) in the basal ganglia represents stable, rather than flexible, object values. After across-day learning of objectreward association, SNr neurons gradually showed a response bias to surprisingly many visual objects: inhibition to high-valued objects and excitation to low-valued objects. Many of these neurons were shown to project to the ipsilateral superior colliculus. This neuronal bias remained intact even after 100 d without further learning. In parallel with the neuronal bias, the monkeys tended to look at high-valued objects. The neuronal and behavioral biases were present even if no value was associated during testing. These results suggest that SNr neurons bias the gaze toward objects that were consistently associated with high values in ones history. The primate ventral pallidum encodes expected reward value and regulates motor action: Motor actions are facilitated when expected reward value is high. It is hypothesized that there are neurons that encode expected reward values to modulate impending actions and potentially represent motivation signals. Here, we present evidence suggesting that the ventral pallidum (VP) may participate in this process. We recorded single neuronal activity in the monkey VP using a saccade task with a direction-dependent reward bias. Depending on the amount of the expected reward, VP neurons increased or decreased their activity tonically until the reward was delivered, for both ipsiversive and contraversive saccades. Changes in expected reward values were also associated with changes in saccade performance (latency and velocity). Furthermore, bilateral muscimol-induced inactivation of the VP abolished the reward-dependent changes in saccade latencies. These data suggest that the VP provides expected reward value signals that are used to facilitate or inhibit motor actions. Selective and graded coding of reward uncertainty by neurons in the primate anterodorsal septal region: Natural environments are uncertain. Uncertainty of emotional outcomes can induce anxiety and raise vigilance, promote and signal the opportunity for learning, modulate economic choice and regulate risk-seeking. Here we demonstrate that a subset of neurons in the anterodorsal region of the primate septum (ADS) are primarily devoted to processing uncertainty in a highly specific manner. Those neurons were selectively activated by visual cues indicating probabilistic delivery of reward (for example, 25%, 50% and 75% reward) and did not respond to cues indicating certain outcomes (0% and 100% reward). The average ADS uncertainty response was graded with the magnitude of reward uncertainty and selectively signaled uncertainty about rewards rather than punishments. The selective and graded information about reward uncertainty encoded by many neurons in the ADS may underlie modulation of uncertainty of value- and sensorimotor-related areas to regulate goal-directed behavior. Reward value-contingent changes of visual responses in the primate caudate tail associated with a visuomotor skill: A goal-directed action aiming at an incentive outcome, if repeated, becomes a skill that may be initiated automatically. We now report that the tail of the caudate nucleus (CDt) may serve to control a visuomotor skill. Monkeys looked at many fractal objects, half of which were always associated with a large reward (high-valued objects) and the other half with a small reward (low-valued objects). After several daily sessions, they developed a gaze bias, looking at high-valued objects even when no reward was associated. CDt neurons developed a response bias, typically showing stronger responses to high-valued objects. In contrast, their responses showed no change when object values were reversed frequently, although monkeys showed a strong gaze bias, looking at high-valued objects in a goal-directed manner. The biased activity of CDt neurons may be transmitted to the oculomotor region so that animals can choose high-valued objects automatically based on stable reward experiences.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Investigator-Initiated Intramural Research Projects (ZIA)
Project #
1ZIAEY000415-11
Application #
8737633
Study Section
Project Start
Project End
Budget Start
Budget End
Support Year
11
Fiscal Year
2013
Total Cost
$1,418,351
Indirect Cost
Name
U.S. National Eye Institute
Department
Type
DUNS #
City
State
Country
Zip Code
Ghazizadeh, Ali; Griggs, Whitney; Hikosaka, Okihide (2016) Object-finding skill created by repeated reward experience. J Vis 16:17
Yasuda, Masaharu; Hikosaka, Okihide (2015) Functional territories in primate substantia nigra pars reticulata separately signaling stable and flexible values. J Neurophysiol 113:1681-96
Kim, Hyoung F; Hikosaka, Okihide (2015) Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards. Brain 138:1776-800
Monosov, Ilya E; Leopold, David A; Hikosaka, Okihide (2015) Neurons in the Primate Medial Basal Forebrain Signal Combined Information about Reward Uncertainty, Value, and Punishment Anticipation. J Neurosci 35:7443-59
Kim, Hyoung F; Ghazizadeh, Ali; Hikosaka, Okihide (2015) Dopamine Neurons Encoding Long-Term Memory of Object Value for Habitual Behavior. Cell 163:1165-75
Hong, S; Hikosaka, O (2014) Pedunculopontine tegmental nucleus neurons provide reward, sensorimotor, and alerting signals to midbrain dopamine neurons. Neuroscience 282:139-55
Proulx, Christophe D; Hikosaka, Okihide; Malinow, Roberto (2014) Reward processing by the lateral habenula in normal and depressive behaviors. Nat Neurosci 17:1146-52
Kim, Hyoung F; Ghazizadeh, Ali; Hikosaka, Okihide (2014) Separate groups of dopamine neurons innervate caudate head and tail encoding flexible and stable value memories. Front Neuroanat 8:120
Gottlieb, Jacqueline; Hayhoe, Mary; Hikosaka, Okihide et al. (2014) Attention, reward, and information seeking. J Neurosci 34:15497-504
Kim, Hyoung F; Hikosaka, Okihide (2013) Distinct basal ganglia circuits controlling behaviors guided by flexible and stable values. Neuron 79:1001-10

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