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Research Articles, Behavioral/Cognitive

Neuronal Activity in the Posterior Cingulate Cortex Signals Environmental Information and Predicts Behavioral Variability during Trapline Foraging

David L. Barack and Michael L. Platt
Journal of Neuroscience 24 March 2021, 41 (12) 2703-2712; DOI: https://doi.org/10.1523/JNEUROSCI.0305-20.2020
David L. Barack
1Departments of Philosophy, Neuroscience, and Economics, Columbia University, New York, New York 10027
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Michael L. Platt
2Departments of Neuroscience, Psychology, and Marketing, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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    Figure 1.

    Monkeys spontaneously trapline, efficiently choosing targets in a circle, when foraging in a circular array but deviate from these routines as the environment becomes better known. A, Recording location in the PCC. Left, Monkey L. Right, Monkey R. B, Traplining task, sample trial sequence. Trials began with monkeys fixating a central cross for a variable amount of time. After fixation offset, six targets appeared in the same locations across trials. Monkeys then chose targets in any order. To register a choice, monkeys fixated targets for 250 ms. Only two rewards, one small and one large, were available on every trial, and the identity of the rewarded targets changed in a pseudorandom fashion from trial to trial. In order to advance to the next trial, monkeys had to select every target. Open circle represents simulated eye position. Dashed arrow indicates direction of impending saccade. Dashed circle represents impending saccade endpoint. Small juice drop represents small reward. Large juice drop represents large reward. Central semi-circle represents step size, the clockwise or counterclockwise distance between subsequently chosen targets. S, Start; −2, two targets counterclockwise; −1, one target counterclockwise; +1, one target clockwise. C, Left, Mean ± SEM BE for high expected environmental information (ΔHE) choices (E[ΔHE] > mean(E[ΔHE])) compared with low expected information choices (E[ΔHE] ≤ mean(E[ΔHE])) across all sessions and choices. Right, Boxplot by CN2-CN5 across sessions before receipt of last informative outcome (E[ΔHE] > 0; red points) and after (E[ΔHE] = 0; green points). Top and bottom of box are interquartile (25%-75%) range of session means. Notch indicates 95% CI for median session. Nonoverlapping notches indicate significantly different medians at α = 0.05. Each point is a session mean. CN2 always possesses some expected information; hence, no green box or points. n = 145,524 choices, 24,254 trials.

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    Figure 2.

    PCC neurons preferentially encode environmental information over reward. A, Firing rate of sample neuron encoding expected information but not expected reward across all CN1-CN6, plotted separately by expected information (E[ΔHE]). Legends indicate expected reward(s) for each plot. Blue line indicates end of saccade. B, Tuning curves for expected information (top) and expected reward (bottom), collapsed across CNs for better visibility, for the cell plotted in A. This example cell showed elevated firing rates for higher amounts of information. The elevated firing rates for certain amounts of expected reward correspond to choices with high expected information with only a single level of expected reward. C, Number of cells encoding expected reward by choice (red) for constant expected information, and number of cells encoding expected information by choice (green). Neurons were included in the expected reward counts if Student t tests (CN2-CN4) or ANOVA (CN5-CN6) indicated a significant difference in firing rates (p < 0.05, uncorrected for multiple comparisons to allow the weakest criteria for inclusion, and the same cell could appear for more than one CN).

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    Figure 3.

    Neurons in PCC forecast deviations in behavior. A, Sample neuron encoding BE during the anticipation epoch. This cell was more active for high entropy choices than for low entropy choices. B, Population encoding of BE. The population was more active for high entropy choices than low. C, Sample cell encoding the end of information gathering. This cell had higher firing rates after the last informative or rewarding outcome compared with before. Thin blue lines with dashed lines very close on either side indicate average time of choice before (left) or after (right) last informative or rewarding choice ± 1 SEM. D, The population also encoded this boundary, with higher firing rates after the last informative or rewarding outcome compared with before. B, D, n = 124 cells. A, B, Blue line indicates end of saccade. C, D, Middle blue line indicates time of outcome. A-D, Shading represents ±1 SEM. *p < 0.05 for that 10 ms time bin.

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    Table 1.

    Equations for expected reward, entropy, information, and expected information for the reward sequence

    Pattern no.Permutation
    p
    Expected reward
    Embedded Image
    Entropy
    Embedded Image
    Information
    Embedded Image
    Expected information
    Embedded Image
    10 0 0 0 1 20.5 0.6 0.75 1.0 1.5 2.00.5850 1.3219 3.3219 3.9069 4.9069 4.90690.5850 0.7370 1 1.5850 1 01.2516 0.7370 1 1.5850 1 0
    20 0 0 0 2 10.5 0.6 0.75 1.0 1.5 1.00.5850 1.3219 3.3219 3.9069 4.9069 4.90690.5850 0.7370 1 1.5850 1 01.2516 0.7370 1 1.5850 1 0
    30 0 0 1 0 20.5 0.6 0.75 1.0 1.0 2.00.5850 1.3219 3.3219 3.9069 4.9069 4.90690.5850 0.7370 1 1.5850 1 01.2516 0.7370 1 1.5850 1 0
    ⫶⫶⫶⫶⫶⫶
    302 1 0 0 0 00.5 0.2 0 0 0 02.5850 4.9069 4.9069 4.9069 4.9069 4.90692.5850 2.3219 0 0 0 01.2516 2.3219 0 0 0 0
    • Each column in the table (except for the leftmost) contains six columns, each corresponding to a CN during the trial. Total number of choices on every trial = 6. |·| represents cardinality of ·; n = CN; i = CN in trial. R, Reward.

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The Journal of Neuroscience: 41 (12)
Journal of Neuroscience
Vol. 41, Issue 12
24 Mar 2021
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Neuronal Activity in the Posterior Cingulate Cortex Signals Environmental Information and Predicts Behavioral Variability during Trapline Foraging
David L. Barack, Michael L. Platt
Journal of Neuroscience 24 March 2021, 41 (12) 2703-2712; DOI: 10.1523/JNEUROSCI.0305-20.2020

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Neuronal Activity in the Posterior Cingulate Cortex Signals Environmental Information and Predicts Behavioral Variability during Trapline Foraging
David L. Barack, Michael L. Platt
Journal of Neuroscience 24 March 2021, 41 (12) 2703-2712; DOI: 10.1523/JNEUROSCI.0305-20.2020
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Keywords

  • cognition
  • exploration
  • foraging
  • information
  • posterior cingulate

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