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A neural mechanism of response bias
Johan LauwereynsLaboratory of Sensorimotor Research
National Eye Institute, NIH
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Yoriko Takikawa Juntendo Univ.Reiko Kawagoe Juntendo Univ.Masashi Koizumi Tamagawa Univ.Shunsuke Kobayashi Tamagawa Univ.Masamichi Sakagami Tamagawa Univ.Brian Coe ATRHiro Nakahara RIKEN
Katsumi Watanabe NIHOkihide Hikosaka NIH
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Goal-oriented behavior:
Seeking salt
(Curt Richter)
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A Neural Mechanism of Reward-oriented Response Bias in the Basal Ganglia
• How does the brain incorporate reward value in the process of response selection?
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A Neural Mechanism of Reward-oriented Response Bias in the Basal Ganglia
• How does the brain incorporate reward value in the process of response selection?
• Anticipatory bias toward reward in the activity of monkey caudate neurons
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A Neural Mechanism of Reward-oriented Response Bias in the Basal Ganglia
• How does the brain incorporate reward value in the process of response selection?
• Anticipatory bias toward reward in the activity of monkey caudate neurons
• Studied using visually and memory-guided saccade tasks with asymmetrical reward schedule
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Biased Saccade Task (BST)
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Biased Saccade Task (BST)
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Biased Saccade Task (BST)
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Saccade-related brain areas (macaque monkey)
FEF: frontal eye fieldSEF: supplementary eye fieldLIP: area LIP of parietal cortexCD: caudate nucleusSNr: substantia nigra pars reticulataSC: superior colliculusClbm: cerebellumSG: brainstem saccade generators
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DA neuron responds to Reward & Reward Predictor
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Inputs to Striatal Medium Spiny Neuron
Smith & Bolam (1990)
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Medium Spiny Neuron in Striatum
Preston, Bishop & Kitai (1980)
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Single unit recording from Caudate Nucleus
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L-CD neuron: R-rewardReward
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L-CD neuron: RL-rewardReward
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L-CD neuron: RLR-rewardReward
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L-CD neuron: AllReward
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Population activity of CD neurons(with contra-bias, n=25)
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Motivational control of Eye Movements by the Basal Ganglia
• How does the selective anticipatory activity in caudate relate to saccade parameters?
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Motivational control of Eye Movements by the Basal Ganglia
• How does the selective anticipatory activity in caudate relate to saccade parameters?
• Basic association between neuronal activity and response latency
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Motivational control of Eye Movements by the Basal Ganglia
• How does the selective anticipatory activity in caudate relate to saccade parameters?
• Basic association between neuronal activity and response latency.
• But what’s the relationship for a given combination of saccade and reward direction?
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Median-split analysis
• Divide the data in two groups of trials for each combination of saccade and reward direction
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Median-split analysis
• Divide the data in two groups of trials for each combination of saccade and reward direction
• High-activity trials, with pretarget activity above the median for that condition
• Low-activity trials, with pretarget activity below the median for that condition
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Discussion
• The data for contra-bias neurons provide evidence in favor of the hypothesis of selective preparation
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Discussion
• The data for contra-bias neurons provide evidence in favor of the hypothesis of selective preparation
• High pretarget activity leads to short latency for saccades in the contralateral direction
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Discussion
• The data for contra-bias neurons provide evidence in favor of the hypothesis of selective preparation
• High pretarget activity leads to short latency for saccades in the contralateral direction
• What about the data for ipsi-bias neurons?
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Discussion (continued)
• The data for ipsi-bias neurons are a mirror-image of the data for contra-bias neurons
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Discussion (continued)
• The data for ipsi-bias neurons are a mirror-image of the data for contra-bias neurons
• High pretarget activity of ipsi-bias neurons leads to long latency for unrewarded saccades in the contralateral direction
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Discussion (continued)
• The data for ipsi-bias neurons are a mirror-image of the data for contra-bias neurons
• High pretarget activity of ipsi-bias neurons leads to long latency for unrewarded saccades in the contralateral direction
• Activity of these neurons disrupts contralateral saccades (“negative motivation”)
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Summary
• The entire pattern of data suggests that the caudate anticipatory bias influences contralateral saccade latency
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Summary
• The entire pattern of data suggests that the caudate anticipatory bias influences contralateral saccade latency
• Contra-bias neurons facilitate contralateral saccades,
Ipsi-bias neurons disrupt contralateral saccades
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Summary
• The entire pattern of data suggests that the caudate anticipatory bias influences contralateral saccade latency
• Contra-bias neurons facilitate contralateral saccades,
Ipsi-bias neurons disrupt contralateral saccades
• These two type of neurons may reflect the physiology of the direct and indirect pathway in the basal ganglia
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Neural Circuit of the Basal Ganglia
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CD
SNr
SC
CD
SNr
SC
Direct pathway: Contra-bias neurons
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CD
SNr
SC
CD
SNr
SC
GPe
STN
GPe
STN
Indirect pathway: Ipsi-bias neurons
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Experiment 2
• The data so far show an effect of selective response preparation on the basis of reward value
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Experiment 2
• The data so far show an effect of selective response preparation on the basis of reward value
• But could this merely reflect a more general type of spatially selective response preparation?
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Experiment 2
• The data so far show an effect of selective response preparation on the basis of reward value
• But could this merely reflect a more general type of spatially selective response preparation?
• Test with a “cognitive bias task”…
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Cognitive Bias Task(delayed position matching)
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CD activity in Cognitive & Motivational TasksCognitive Bias
Motivational Bias
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Motivational Bias
Cog
nit
ive
Bia
sMost CD neurons show higher
Motivational Bias than Cognitive Bias
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Experiment 3
• We’ve provided evidence for an effect of spatially selective reward-oriented response preparation
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Experiment 3
• We’ve provided evidence for an effect of spatially selective reward-oriented response preparation
• But is the reward-oriented bias really related to motor preparation or is it involved in more abstract or perceptual decision making?
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Experiment 3
• We’ve provided evidence for an effect of spatially selective reward-oriented response preparation
• But is the reward-oriented bias really related to motor preparation or is it involved in more abstract or perceptual decision making?
• Test with a memory-guided eye movement task with color-based reward association…
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Discussion (Exp. 3)
• Color-reward associations do lead to significant effects in both behavior and caudate activity
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Discussion (Exp. 3)
• Color-reward associations do lead to significant effects in both behavior and caudate activity
• The anticipatory activity is aimed at the visual onset, not the start of the eye movement
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Discussion (Exp. 3)
• Color-reward associations do lead to significant effects in both behavior and caudate activity
• The anticipatory activity is aimed at the visual onset, not the start of the eye movement
• If this is indeed a ‘perceptual’ process, then how does the bias affect the neuronal activity to the visual target?
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Discussion (Exp. 3; continued)
• Strong pre-cue activity leads to general increase, not improved discriminability
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Discussion (Exp. 3; continued)
• Strong pre-cue activity leads to general increase, not improved discriminability
• Different from cortical mechanisms of visual attention: here additive, not multiplicative scaling
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Discussion (Exp. 3; continued)
• Strong pre-cue activity leads to general increase, not improved discriminability
• Different from cortical mechanisms of visual attention: here additive, not multiplicative scaling
• Analogous to a shift of decision criterion?
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Conclusion
• Anticipatory activity in caudate nucleus is influenced by the context of stimulus-reward mapping
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Conclusion
• Anticipatory activity in caudate nucleus is influenced by the context of stimulus-reward mapping
• This activity can create a spatially selective bias that prioritizes an action with high reward value
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Conclusion
• Anticipatory activity in caudate nucleus is influenced by the context of stimulus-reward mapping
• This activity can create a spatially selective bias that prioritizes an action with high reward value
• The bias also affects visual processing;Does this bias incorporate reward value
in the process of perceptual decision making?
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Future directions
• Motivational control of visual processing in humans:
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Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
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Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
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Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
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Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
– Parkinsonian patients
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Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
– Parkinsonian patients
– Feedback to monkey studies (design, analysis, modeling)
![Page 76: A neural mechanism of response bias Johan Lauwereyns Laboratory of Sensorimotor Research National Eye Institute, NIH](https://reader036.vdocuments.mx/reader036/viewer/2022070402/56649f265503460f94c3d33a/html5/thumbnails/76.jpg)
Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
– Parkinsonian patients
– Feedback to monkey studies (design, analysis, modeling)
• Pharmacological study of motivational control:
![Page 77: A neural mechanism of response bias Johan Lauwereyns Laboratory of Sensorimotor Research National Eye Institute, NIH](https://reader036.vdocuments.mx/reader036/viewer/2022070402/56649f265503460f94c3d33a/html5/thumbnails/77.jpg)
Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
– Parkinsonian patients
– Feedback to monkey studies (design, analysis, modeling)
• Pharmacological study of motivational control:– Create a rat model of the Biased Response Task
![Page 78: A neural mechanism of response bias Johan Lauwereyns Laboratory of Sensorimotor Research National Eye Institute, NIH](https://reader036.vdocuments.mx/reader036/viewer/2022070402/56649f265503460f94c3d33a/html5/thumbnails/78.jpg)
Future directions
• Motivational control of visual processing in humans:– Response bias, decision bias, perceptual sensitivity
– Systematic comparison with ‘visual attention’
– Modeling (LATER, ROC)
– Parkinsonian patients
– Feedback to monkey studies (design, analysis, modeling)
• Pharmacological study of motivational control:– Create a rat model of the Biased Response Task
– Study the neurochemical make-up of this system