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Research Articles, Systems/Circuits

Choice-Selective Neurons in the Auditory Cortex and in Its Striatal Target Encode Reward Expectation

Lan Guo, Jardon T. Weems, William I. Walker, Anastasia Levichev and Santiago Jaramillo
Journal of Neuroscience 8 May 2019, 39 (19) 3687-3697; DOI: https://doi.org/10.1523/JNEUROSCI.2585-18.2019
Lan Guo
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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Jardon T. Weems
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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William I. Walker
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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Anastasia Levichev
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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Santiago Jaramillo
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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  • Figure 1.
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    Figure 1.

    Expected reward size biases sound-driven choices. A, Two-alternative choice sound-discrimination task with changing reward. The amount of reward delivered by each side port changed in alternating blocks of 150–200 trials. B, Average psychometric curve from one mouse (6 sessions) showing a bias toward the port with larger reward. Performance for additional sessions in which both ports delivered the same amount of reward is shown in gray for comparison. Error bars indicate 95% confidence intervals. C, Average performance on each reward contingency for each mouse tested (11 mice, 6 sessions each). Larger reward on the right port led to a higher percentage of rightward choices for the lowest sound frequency: 6.2 kHz (left), the frequency at the decision boundary: 10.9 kHz (middle), and the highest frequency: 19.2 kHz (right). Stars indicate p ≤ 0.01.

  • Figure 2.
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    Figure 2.

    Reward expectation does not alter reaction times or movement times. A, Reaction time on each trial was defined as the time between the end of the sound stimulus and the exit from the center port. B, Average reaction times on each reward contingency for each mouse (11 mice, 6 sessions each mouse) on trials with leftward choices. C, Reaction time as in B for rightward choices. D, Movement time on each trial was defined as the time between the exit from the center port and the entry to a side port. E, Average movement times for each mouse for leftward choices. F, Average movement times for rightward choices. No statistical significance (p ≥ 0.05) is indicated by n.s.

  • Figure 3.
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    Figure 3.

    Activity of neurons from AC and pStr was selective to sound stimuli during the task. A, Coronal brain slices showing recording tracks for the AC (green). Red lines indicate the tracks of movable tetrode bundles used for recordings. B, Coronal brain slice showing recording tracks for the posterior striatum (yellow). C, Responses to sound stimuli of 8 and 19.2 kHz in the task for an example cell from the AC. D, Responses to sound stimuli of 8 and 15 kHz in the task for a striatal cell. The box plots above the spike raster show the distributions of center-port exit times.

  • Figure 4.
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    Figure 4.

    Reward expectation modulates sound-evoked responses in AC and pStr. A, Responses of an auditory cortical neuron to a sound stimulus as reward amount changed during the task (3 blocks of trials shown). Sound-evoked responses were modulated by the size of expected reward. The box plot above the spike raster shows the distribution of center-port exit times. B, Responses modulated by expected reward size, as in A, for a posterior striatal neuron (four blocks of trials shown). C, Activity of a different AC neuron showing no influence of reward expectation on the sound-evoked response. D, Activity of a different posterior striatum neuron not influenced by the expected reward size. E, F, Influence of reward expectation on sound-evoked activity for all neurons responsive to stimuli in the task. Neuron with statistically significant modulation (p ≤ 0.05, Wilcoxon rank sum test), are shown in black.

  • Figure 5.
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    Figure 5.

    Neural activity in AC and pStr encodes choice direction. A, Example neuron from the AC showing different levels of activity when the mouse traveled to the left port versus the right port. Average firing aligned to movement onset for correct trials (790 trials) and error trials (41 trials) show similar patterns of activity when the animal moves in a given direction independent of the sound. The box plots above the spike raster show the distributions of sound-onset times (before movement) and side-port entry times (after movement). B, Similar to A for a cell recorded in the posterior striatum (509 correct trials, 125 error trials). C, D, Choice direction selectivity during movement for all recorded neurons in AC and pStr, respectively. Cells with statistically significant selectivity to choice direction (p ≤ 0.05, Wilcoxon rank sum test) are shown in black.

  • Figure 6.
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    Figure 6.

    Time of maximal selectivity to choice direction is distributed along the movement period. A, Choice selectivity as a function of time for each choice-selective cortical cell (each row is 1 cell), calculated in 10 ms windows during the movement period. Cells are grouped based on whether their maximum selectivity index is positive or negative, and sorted by the time of maximum selectivity. A positive index indicates that activity was larger for movements contralateral to the recording site. B, Similar to A, for choice-selective neurons in the posterior striatum.

  • Figure 7.
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    Figure 7.

    Reward expectation modulates choice-selective activity in AC and pStr. A, Activity of an auditory cortical neuron during movement to one reward port as reward amount changed during the task. Choice-selective activity was modulated by the size of expected reward. The box plots above the spike raster show the distributions of sound-onset times (before movement) and side-port entry times (after movement). B, Activity modulated by expected reward size, as in A, for a posterior striatal neuron. C, Activity of a different AC neuron showing no influence of reward expectation on choice-selective activity. D, Activity of a different posterior striatum neuron not influenced by the expected reward size. E, F, Influence of reward expectation on activity during movement (0–300 ms after center port exit) for all choice-selective neurons in AC and pStr, respectively. Cells with statistically significant selectivity to choice direction (p ≤ 0.05, Wilcoxon rank sum test) are shown in black.

  • Figure 8.
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    Figure 8.

    Time of maximal modulation by reward expectation is distributed along the movement period. A, Modulation by reward expectation for each choice-selective cortical cell (each row is 1 cell), calculated in 10 ms windows during the movement period. Cells are grouped based on whether their maximum modulation is positive or negative, and sorted by the time of maximum modulation. B, Similar to A, for choice-selective neurons in the posterior striatum.

  • Figure 9.
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    Figure 9.

    Neurons in AC and pStr rapidly changed firing after changes in reward contingency. A, Change in the fraction of rightward choices after a change in reward contingency for animals with AC recordings. The plot shows the average across all animals and all block switches (gray line). The data for each session was normalized to the average of rightward choices before averaging. The solid lines show the average values before the switch (red) and after the switch (blue). The fraction of choices reaches an asymptote at ∼10 trials. B, Change in activity during movement for reward-modulated AC neurons after a change in reward contingency. Only data for each cell's preferred choice is used in this analysis. For each cell, the mean firing during the movement period was subtracted and the result was divided by the SD of the activity before the switch. The gray line shows the average across all modulated cells. The solid lines show averages before (red) and after (blue) the switch. C, Same as A for animals with pStr recordings. D, Same as B for pStr neurons.

  • Figure 10.
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    Figure 10.

    Correlation of modulation magnitudes between different factors and time periods. A, Spearman correlation between estimated modulation indices across cells in AC. Absolute values of the indices are used in the calculation. Statistically significant correlations (p < 0.05) are shown in bold. B, Same as in A but for pStr neurons.

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The Journal of Neuroscience: 39 (19)
Journal of Neuroscience
Vol. 39, Issue 19
8 May 2019
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Choice-Selective Neurons in the Auditory Cortex and in Its Striatal Target Encode Reward Expectation
Lan Guo, Jardon T. Weems, William I. Walker, Anastasia Levichev, Santiago Jaramillo
Journal of Neuroscience 8 May 2019, 39 (19) 3687-3697; DOI: 10.1523/JNEUROSCI.2585-18.2019

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Choice-Selective Neurons in the Auditory Cortex and in Its Striatal Target Encode Reward Expectation
Lan Guo, Jardon T. Weems, William I. Walker, Anastasia Levichev, Santiago Jaramillo
Journal of Neuroscience 8 May 2019, 39 (19) 3687-3697; DOI: 10.1523/JNEUROSCI.2585-18.2019
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Keywords

  • auditory
  • expectation
  • flexibility
  • motor
  • reward
  • striatum

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