Yuri Imaizumi’s research while affiliated with University of Tsukuba and other places

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Publications (21)


Fast-spiking neurons in monkey orbitofrontal cortex underlie economic value computation
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April 2025

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9 Reads

Tomoaki Murakawa

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Takashi Kawai

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Yuri Imaizumi

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Inhibitory interneurons are fundamental constituents of cortical circuits that process information to shape economic behaviors. However, the role of inhibitory interneurons in this process remains elusive at the core cortical reward-region, orbitofrontal cortex (OFC). Here, we show that presumed parvalbumin-containing GABAergic interneurons (fast-spiking neurons, FSNs) cooperate with presumed regular-spiking pyramidal neurons (RSNs) during economic-values computation. While monkeys perceived a visual lottery for probability and magnitude of rewards, identified FSNs occupied a small subset of OFC neurons (12%) with high-frequency firing-rates and wide dynamic-ranges, both are key intrinsic cellular characteristics to regulate cortical computation. We found that FSNs showed higher sensitivity to the probability and magnitude of rewards than RSNs. Unambiguously, both neural populations signaled expected values (i.e., probability times magnitude), but FSNs processed these reward's information strongly governed by the dynamic range. Thus, cooperative information processing between FSNs and RSNs provides a common cortical framework for computing economic values.

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Figure 1. Neural population geometries in the visual memory pathway (A) Anatomical depiction of neural populations obtained from the 10 brain regions in nine macaques during the four different behavioral tasks in Exps. 1 to 4. (B-E) Rotational (B), curvy (C), straight (D), and unclear dynamics (E) detected by visual inspection. Single trajectory geometry was obtained in each brain region using neural population data. Number of neurons were 116-590 (Table S1). In A-E, the 10 brain regions are numbered as follows: 1. TE, 2. STRt, 3. PRC, 4. CDb, 5. HPC, 6. VS, 7. cOFC, 8. CDh&b, 9. PHC, and 10. mOFC. The 0.05 s time bin was used for the analysis. The time from visual stimulus appearance was shown in sec. Characters indicate stimulus conditions; Ib: best item; I2 to I7: second best to seventh best item; Iw: worst item; D: delay, M: magnitude; P: probability. See also Figures S1-S3 and Table S1.
Figure 2. Quantitative evaluation of geometric structures according to the rotational features (A) Schematic depictions of the estimation of accumulated angle difference weighted by the deviance, Sdq. The accumulated angle difference indicates the degree of geometric change in terms of the rotational force across time. Vector distance (d), rotational speed (q/0.1s), and start to endpoint distance (d S-E ) were also estimated. (B) Dendrogram estimated from these four parameter values based on bootstrap resampling across 10 neural populations. (C) Percentage of variance explained by PCA of bootstrap resampling data across 10 neural populations. (D) Clusters detected among the four parameters based on the PCA. Dots represent replicates composed of 20,000 (1000 replicates in each 10 brain regions times two task conditions). (E) Percentage of the identified clusters in each of the 10 brain regions. Each neural population contained two components of neural information: the best (B) and worst (W) conditions in Exps. 1 and 3, magnitude (M) and delay (D) of the rewards in Exp. 2, and magnitude (M) and probability (P) of rewards in Exp. 4. Colors on the atlas indicate geometry types on visual inspection in Figure 1A.
Figure 4. Summary of the observed dynamics and anatomical connections in the visual memory pathway (A) Geometries depicted in the same arbitrary scales on the PC1-2 plane for the eight neural populations shown in Figures 1B-1D. The start of the trajectory (S) is aligned to describe each trajectory. e indicates the end of the trajectory at 0.6 s. (B) Proportion of the clusters defined in each of the 10 brain regions are described with the anatomical connection. Reddish: rotational, greenish: curvy, bluish: straight dynamics. Data from CDh&b and CDb are merged (CD).
Formation of brain-wide neural geometry during visual item recognition in monkeys

January 2025

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108 Reads

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1 Citation

iScience

He Chen

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[...]

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Formation of brain-wide neural geometry during visual item recognition in monkeys

August 2024

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51 Reads

Neural dynamics reflect canonical computations that relay and transform information in the brain. Previous studies have identified the neural population dynamics in many individual brain regions as a trajectory geometry in a low-dimensional neural space. However, whether these populations share particular geometric patterns across brain-wide neural populations remains unclear. Here, by mapping neural dynamics widely across temporal/frontal/limbic regions in the cortical and subcortical structures of monkeys, we show that 10 neural populations, including 2,500 neurons, propagate visual item information in a stochastic manner. We found that the visual inputs predominantly evoked rotational dynamics in the higher-order visual area, the TE and its downstream striatum tail, while curvy/straight dynamics appeared more frequently downstream in the orbitofrontal/hippocampal network. These geometric changes were not deterministic but rather stochastic according to their respective emergence rates. These results indicated that visual information propagates as a heterogeneous mixture of stochastic neural population signals in the brain.




Figure 3. Example activity of neurons during the single-cue and ILR tasks. A, An example activity histogram of a cOFC neuron modulated by the probability and magnitude of rewards during the single-cue task. Activity aligned with cue onset is represented for three different levels of probability (P, 0.1-0.3, 0.4-0.7, 0.8-1.0) and magnitude (M, 0.1-0.3 ml, 0.4-0.7 ml, 0.8-1.0 ml) of rewards. Gray hatched areas indicate the 1 s time window used to estimate the neural firing rates shown in B. Histograms smoothed using a Gaussian kernel (s ¼ 50 ms). B, An activity plot of the cOFC neuron during the 1 s time window shown in A against the probability and magnitude of rewards. C, The percentage of neural modulation types detected in 1 s time window shown in A: the P, M, Both, and NO. D, Percentages of neural modulation type detected in the 0.02 s time bins during the 1.0 s after cue onset. Calibration: 0.2 s. E, Regression coefficient plots for the probability and magnitude of rewards estimated for all cOFC neurons in Exp. 1. Regression coefficients in the 0.02 s time bin shown every 0.1 s during the 0.6 s after cue onset (0-0.02 s, 0.10-0.12 s, 0.20-0.22 s, 0.30-0.32 s, 0.40-0.42 s, 0.50-0.52 s, and 0.58-0.60 s). Filled gray indicates significant regression coefficient for either Probability or Magnitude at p , 0.05. F, An example of an HPC neuron showing sample-triggered sample-location signals and item signals. A 0.08-1.0 s time window after sample onset was used to estimate the neural firing rates shown in G. Histograms are smoothed using a Gaussian kernel (s ¼ 20 ms). G, An activity plot of the HPC neuron during the time window shown in F against item and location. H, The percentage of neural modulation types detected in the 0.08-1.0 s window shown in F; Item, Location, Both, and NO. I, Percentages of neural modulation types detected in the 0.02 s time bins during the 1.0 s after sample onset. J, Regression coefficient plots for the best and worst items estimated for all HPC neurons in Exp. 2. Filled gray indicates significant regression coefficient for item at p , 0.05 using ANOVA without interaction term. The location modulation was not shown because we showed changes of neural modulation by the sample stimulus, whereas the location had already been provided to the monkeys. A, B, and D were published previously in the study by Yamada et al. (2021).
Figure 4. Graphic methods for the conventional rate-coding analysis and state-space analysis in the regression subspace. Conventional analysis (top and middle rows): in each single neuron, activity modulations by task variables are detected in the fixed time window (top row) using linear regression and ANOVA for continuous (left, Exp. 1) and categorical (right, Exp. 2) task parameters (Fig. 2, see for the task details), respectively. The same analyses were applied in a fine time resolution in Exp. 1 and Exp. 2 (middle row). The conventional analyses using a general linear model (linear regression and ANOVA) provide the extent of neural
Figure 5. The state-space analysis provides a temporal structure of neural modulation in the cOFC. A, Cumulative variance explained by PCA in the cOFC population. The arrowhead indicates the percentage of variance explained by PC1 and PC2. B, Time series of eigenvectors, PC1 to PC3 in the cOFC population. C, A series of eigenvectors for PC1 to PC3 are plotted against PC1 and PC2, and PC2 and PC3 dimensions in the cOFC population. Plots at the beginning and end of the series of vectors are labeled as start (s) and end (e), respectively. a.u., Arbitrary unit.
Figure 6. Temporal structure of neural modulation in the HPC population. A, Cumulative variance explained by PCA in the HPC population. The arrowhead indicates the percentages of variances explained by PC1 and PC2. B, Time series of eigenvectors for six items in the HPC population. The top three PCs are shown. C, Time series of eigenvectors for four locations. D, A series of eigenvectors for PC1 to PC3 are plotted against PC1 and PC2, and PC2 and PC3 dimensions in the HPC population. a.u., Arbitrary unit. Extended Data Figure 6-1 represents shuffled control results.
Figure 8. Quantitative evaluations of eigenvector properties in the cOFC and HPC populations. A, Time series of vector size estimated in the cOFC population for P and M of rewards. Vector sizes are estimated in the PC1-PC2 plane (top) and PC2-PC3 plane (bottom), respectively. a.u., Arbitrary unit. The solid-colored lines indicate interpolated lines using a cubic spline function to provide a resolution of 0.005 s. B, Time series of vector size estimated in the HPC population for the best and worst items. C, Boxplots of vector size estimated in the cOFC population for probability and magnitude of rewards. D, Boxplots of vector size in the HPC population for the best and worst items and locations. E, F, Boxplots of vector angle estimated in the cOFC (E) and HPC (F) populations. G, H, Boxplots of vector deviance from the mean estimated in the cOFC (G) and HPC (H) populations. In C-H, data after 0.1 s are used. *p , 0.05, ***p , 0.001.
Stable Neural Population Dynamics in the Regression Subspace for Continuous and Categorical Task Parameters in Monkeys

June 2023

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205 Reads

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2 Citations

eNeuro

Neural population dynamics provide a key computational framework for understanding information processing in the sensory, cognitive, and motor functions of the brain. They systematically depict complex neural population activity, dominated by strong temporal dynamics as trajectory geometry in a low-dimensional neural space. However, neural population dynamics are poorly related to the conventional analytical framework of single-neuron activity, the rate-coding regime that analyzes firing rate modulations using task parameters. To link the rate-coding and dynamic models, we developed a variant of state-space analysis in the regression subspace, which describes the temporal structures of neural modulations using continuous and categorical task parameters. In macaque monkeys, using two neural population datasets containing either of two standard task parameters, continuous and categorical, we revealed that neural modulation structures are reliably captured by these task parameters in the regression subspace as trajectory geometry in a lower dimension. Furthermore, we combined the classical optimal-stimulus response analysis (usually used in rate-coding analysis) with the dynamic model and found that the most prominent modulation dynamics in the lower dimension were derived from these optimal responses. Using those analyses, we successfully extracted geometries for both task parameters that formed a straight geometry, suggesting that their functional relevance is characterized as a unidimensional feature in their neural modulation dynamics. Collectively, our approach bridges neural modulation in the rate-coding model and the dynamic system, and provides researchers with a significant advantage in exploring the temporal structure of neural modulations for pre-existing datasets.




Fig. 1. Lottery choice task and monkey choice behavior. (A) A sequence of events in choice trials. Two pie charts representing the available options were presented to the monkeys on the left and right sides of the screen. Monkeys chose either target by fixating on the side where it appeared. (B) Payoff matrix. Each magnitude was fully crossed with each probability, resulting in a pool of 100 lotteries from which two were randomly allocated to the left-and right-side target options on each trial. Expected values (EVs) are calculated in milliliters. (C) The frequency with which the target on the right side was selected for the expected values of the left and right target options. (A) and (C) are published in (26).
Fig. 2. Model estimates for monkeys and humans. (A) BIC values of the standard economic models: EV, EU, TK, P1, GE, and P2. See Materials and Methods for details; monkey SUN (top), monkey FU (middle), and human participants (bottom). The respective color for each model is presented. (B) Illustration of the estimated utility functions in all models. For illustrative purposes and to capture the same range of utility values on the y axis, the x axis is limited to 0 and 1 for humans to allow for an easier comparison with monkeys' utility functions. See fig. S4 for utility over 0 to 5 range. Gray, black, red, purple, green, and orange dashed lines indicate EV, EU, TK, P1, GE, and P2 models, respectively. (C) Illustration of the estimated probability weighting functions in all models.
Fig. 3. Value function and its RPE estimated by using the reinforcement learning model. (A) Plots of the V(p,m) t=10,000 against the expected value defined mathematically, i.e., probability time magnitude. (B) r − V(p,m) t=10,000 after reward plotted against the positive component of RPE, i.e., obtained reward magnitude minus the expected values. (C) r − V(p,m) t=10,000 after no-reward (hence, r is zero) plotted against the negative component of RPE, i.e., zero minus expected value. Plots were made for all stimuli, as a function of different learning rates. r is the correlation coefficient.
Fig. 4. The effect of the RPE through utility and probability weighting functions in the dynamic prospect theory model. Effect of RPE on the utility function (A) and probability weighting function (B) for monkey SUN (top), monkey FU (middle), and human participants (bottom). All curves were drawn using the estimates from Table 4 (model 2). Solid orange lines are drawn assuming the largest RPE (0.9 for monkeys and 4.5 for humans), dashed orange lines are drawn assuming the smallest RPE (−0.9 for monkeys and −4.5 for humans), and the dotted gray line represents RPE = 0. Note that in humans, the dotted gray and dashed orange curves overlap in (A). For illustrative purposes, we limited the y axis and x axis to 0 and 1 for humans to allow for an easier comparison with monkeys' utility functions.
Dynamic prospect theory: Two core decision theories coexist in the gambling behavior of monkeys and humans

May 2023

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168 Reads

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8 Citations

Science Advances

Research in the multidisciplinary field of neuroeconomics has mainly been driven by two influential theories regarding human economic choice: prospect theory, which describes decision-making under risk, and reinforcement learning theory, which describes learning for decision-making. We hypothesized that these two distinct theories guide decision-making in a comprehensive manner. Here, we propose and test a decision-making theory under uncertainty that combines these highly influential theories. Collecting many gambling decisions from laboratory monkeys allowed for reliable testing of our model and revealed a systematic violation of prospect theory's assumption that probability weighting is static. Using the same experimental paradigm in humans, substantial similarities between these species were uncovered by various econometric analyses of our dynamic prospect theory model, which incorporates decision-by-decision learning dynamics of prediction errors into static prospect theory. Our model provides a unified theoretical framework for exploring a neurobiological model of economic choice in human and nonhuman primates.



Citations (5)


... These neural properties might be related to the larger changes in carried information as a function of firing rates and dynamic range ( Figure 4B, compare FSNs and RSN regression slopes, Figure 4C, red). As a result, the output neurons in cortical (9, 10, 12, 13) and subcortical (40)(41)(42)(43) structures becomes active via feedforward inhibition ( Figure 4A) during economic behavior. ...

Reference:

Fast-spiking neurons in monkey orbitofrontal cortex underlie economic value computation
Formation of brain-wide neural geometry during visual item recognition in monkeys

iScience

... Indeed, cortical inhibitory dysfunction results in various diseases including mental disorders (6,7). Since excitatory neurons constitute the majority of neurons at the core cortical center, the orbitofrontal cortex (OFC), they have been well examined in relation to economic behavior to obtain rewards (8)(9)(10)(11)(12)(13)(14). ...

Stable Neural Population Dynamics in the Regression Subspace for Continuous and Categorical Task Parameters in Monkeys

eNeuro

... However, as captured in expected utility theory, decisionmakers are usually not indifferent; they have risk preferences. Tversky and Kahneman (1981) introduced these kinds of problems to illustrate critical tests of divergent predictions of expected utility theory versus prospect theory, still both widely used theories today (e.g., Barberis, 2013;Tymula et al., 2023). Prospect theory predicted gain-loss differences in risk preference, which was thought to rule out expected utility theory in its classic form. ...

Dynamic prospect theory: Two core decision theories coexist in the gambling behavior of monkeys and humans

Science Advances

... In general, we examine the outcome of our choice and adjust subsequent choice behavior using the outcome information to choose an appropriate action. Five significant studies on neurons (Kawai et al. (2015); Yamada et al. (2021); Imaizumi et al. (2022); Yang et al. (2022); Ferrari-Toniolo and Schultz (2023)) have examined neuronal responses to loss and gain. These studies suggest that two different neural systems may respond to loss and gain, resulting in a value function with a cusp as a reference point. ...

A neuronal prospect theory model in the brain reward circuitry

... In a previous study using a choice task, we showed that amygdala neurons do encode subjective values that reflected integrated reward probability and magnitude when these reward attributes were cued simultaneously 12 . Perhaps neurons in the prefrontal cortex, including the orbitofrontal cortex, and parietal cortex might be relatively more important in signaling to accumulate decision variables derived from sequential or otherwise complex cues 28,[63][64][65][66] . Some previous studies found largely similar coding of values and choices in the amygdala and orbitofrontal cortex 13,67 , while others emphasized differences in the time courses with which neurons in these structures track changing values 53,68 , and in the specificity with which single neurons encode complex, multisensory food rewards 69 . ...

Neural Population Dynamics Underlying Expected Value Computation

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience