Hyoung F. Kim, Hidetoshi Amita, Okihide Hikosaka  Neuron 

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Indirect Pathway of Caudal Basal Ganglia for Rejection of Valueless Visual Objects  Hyoung F. Kim, Hidetoshi Amita, Okihide Hikosaka  Neuron  Volume 94, Issue 4, Pages 920-930.e3 (May 2017) DOI: 10.1016/j.neuron.2017.04.033 Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 1 CDt Projection to Caudal-Ventral Region of GPe (A) Scheme of injection sites in CDt in monkey ZO. CTB488 and CTB555 were injected in anterior and posterior regions of CDt, respectively. (B) Injection sites in the anterior and posterior CDt. Fluorescent signals were detected in each region of CDt (white arrows). (C and E) Examples of axon terminal signals in GPe. Axonal plexus (green and red signals) were detected in coronal slices of GPe. White bar: 5 mm. (D) CDt projection sites in coronal slices of GPe. Axon terminals of CDt neurons were mainly found in caudal-ventral regions of GPe (cvGPe). (F) Sagittal view of CDt-projection site in GPe. CTB555 and CTB488 signals were topographically organized in rostral-caudal axis of GPe. Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 2 Visual Neurons in GPe (A) Locations of visually responsive neurons in sagittal view. D, dorsal; V, ventral; R, rostral; C, caudal. Neuronal distributions are projected to rostral-caudal axis (down) and dorsal-ventral axis (right). Number 0 indicates the rostral and dorsal ends of GPe. (B) An example visual response of GPe neuron. One object was presented in contralateral and ipsilateral hemifields to the recording site (left). The example neuron showed inhibitory response to the object presented in contralateral field (middle) but no response to the same one presented in ipsilateral field (right). (C) Comparison between the responses to contralateral objects (abscissa) and ipsilateral objects (ordinate) for individual neurons. The response was determined by the change in activity from the baseline period (−400–0 ms before object presentation) to the test period (50–400 ms after object presentation). (D) Population response of two types of visual neurons. Average neuronal responses (shown by peristimulus time histogram [PSTH]) are aligned on the time of object presentation (0–400 ms). (E–G) Electrophysiological properties of visual and non-visual neurons in GPe. Visual and non-visual neurons had similar spike shapes (E) and baseline activity (F). However, visual GPe neuron had lower inter-trial-interval irregularity than non-visual neurons (G) (mean ± SD, ∗p < 0.05). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 3 Stable Value Coding for Habitual Behavior in cvGPe (A) Object-reward associative learning. An example set of fractal objects that were associated with stable values. During long-term learning, half of objects were associated with a reward (good objects), while the other objects were associated with no reward (bad objects). (B) Free viewing procedure for testing habitual gaze to previously learned objects. Four of eight objects in one set (as in A) was presented, and the monkey freely looked at it without direct reward outcome. After long-term learning (>4 day) and more than 1-day retention, the monkeys showed gaze preference for the good objects (mean ± SE). (C) Passive viewing task to test neuronal response to learned objects. While the monkey fixated at a central white dot, two to six fractal objects were pseudorandomly chosen from a set of eight objects and were sequentially presented in the neurons’ preferred location. (D) An example GPe neuron encoding stable object value. Shown are its responses to eight long-term learned objects (left) and the average responses to good objects (red) and bad objects (blue) (right). (E) Location of a stable value-coding neuron in GPe, indicated by a marking lesion (black arrow) in a Nissl-stained coronal section. Another marking lesion was made 1 mm above the neuron (black arrowhead). The marking lesions were located in the CDt projection area shown in Figure 1D (right). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 4 Population Activity Of Stable Value Coding in GPe (A) Stable value discrimination of visual GPe neurons. For each neuron, the difference in response to good and bad objects was calculated as ROC area. ROC > 0.5: Good > Bad, ROC < 0.5: Bad > Good. Gray area indicates neurons that showed statistically significant stable value coding. (B) Comparison between responses to good objects (abscissa) and bad objects (ordinate) in passive viewing task for visual GPe neurons. The response was determined by the change in activity from the baseline to test period (as in Figure 2C). (C) Population response of visual GPe neurons to learned objects in passive viewing task. Green line indicates the value coding (i.e., good – bad) (mean ± SE). (D) Locations of stable value-coding neurons in sagittal view. D, dorsal; V, ventral; R, rostral; C, caudal. Neuronal distributions are projected to rostral-caudal axis (down) and dorsal-ventral axis (right). Number 0 indicates the rostral or dorsal border of GP. (E) Comparison between response to flexible (abscissa) and stable (ordinate) value coding for individual neurons. ROCs indicate the value discrimination calculated with neuronal responses in passive viewing task (Figure 3C) and flexible value task (Figure S2A). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 5 Convergence of Direct and Indirect Pathways in cdlSNr (A) Tracer injection site in cvGP in monkey AX. CTB555 was injected while single-unit recording of a stable value-coding GPe neuron, and the injection site was found in cvGPe (white arrow). (B) An example slice of cvGPe projection site in SNr. Axon terminal labeled by CTB555 (red) was found in lateral region of SN. (C) GPe projection sites in coronal slices of SNr. Axon terminals of CDt neurons were mainly found in caudal-dorsal-lateral region of SNr (cdlSNr). (D) Scheme of injection sites in cvGPe and CDt. CTB555 was injected in cvGPe or CDt of different monkeys. (E) Injection site in CDt in monkey ZO. CTB555 signal was indicated by white arrow. (F) An example slice of CDt projection site in SNr. CTB555 signal (red) was also detected in lateral region of SN. (G) CDt projection sites in coronal slices of SNr. Axon terminals of CDt neurons were found in caudal-dorsal-lateral region of SNr (cdlSNr). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 6 Double Inhibitions and Flipped Value Coding in CDt-cvGPe-cdlSNr Indirect Pathway (A) Experiment to study the orthodromic stimulation effects along the indirect pathway. CDt, caudate tail. cvGPe, caudal-ventral globus pallidus external segment. cdlSNr, caudal-dorsal-lateral substantia nigra pars reticulata. (B) Orthodromic responses of cvGPe neurons by CDt stimulation. Average activity of 20 neurons. (C and D) Stable value discrimination of the orthodromically responsive GPe neurons. (C) Population response (same format as Figure 4C). (D) Value discrimination of individual neurons (same format as Figure 4A). (E) Orthodromic responses of cdlSNr neurons by cvGPe stimulation. Average activity of 13 neurons. (F and G) Stable value discrimination of the orthodromically responsive cdlSNr neurons. Green line indicates the value coding (i.e., good – bad) (mean ± SE). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 7 Stable Value-Coding cvGPe Neurons Project to cdlSNr Directly (A) Experiment to study the antidromic stimulation effects for the cvGPe-cdlSNr connection. (B) A cvGPe neuron activated antidromically by electrical stimulation in cdlSNr with a fixed latency of 0.6 ms (top). This activation was eliminated when CDt stimulation occurred within 1.06 ms after a spontaneous spike (bottom), confirming its antidromic nature (collision test). (C and D) Stable value discrimination of the antidromically responsive cvGPe neurons. (C) Value discrimination of individual neurons. (D) Population responses, shown separately for positive-coding neurons (left, n = 6) and negative-coding neurons (right, n = 2). Green lines indicate the value coding (i.e., good – bad) (mean ± SE). Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions

Figure 8 Direct and Indirect Pathways to Determine the Goal of Saccadic Eye Movement Differential information processing through direct and indirect pathways. In this scheme, inhibitory and excitatory neurons are shown by black and white circles, respectively. CDt neurons process visual objects selectively, together with their positions and stable reward values (Kim and Hikosaka, 2013; Yamamoto et al., 2013). This set of information is then processed through its direct pathway (CDt-cdlSNr) and indirect pathway (CDt-cvGPe-cdlSNr). Both pathways are sensitive to stable (not flexible) reward values of visual objects, but in opposite manners: direct pathway sensitive to good (historically high-valued) objects, indirect pathway sensitive to bad (historically low-valued) objects. The information on good objects leads to a disinhibition of saccadic neurons in SC (through the direct pathway), facilitating saccades to good objects. The information on bad objects leads to an enhanced inhibition of saccadic neurons in SC (through the indirect pathway), suppressing saccades to bad objects. Neuron 2017 94, 920-930.e3DOI: (10.1016/j.neuron.2017.04.033) Copyright © 2017 Elsevier Inc. Terms and Conditions