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Featured ArticleArticles, Behavioral/Systems/Cognitive

Attention for Learning Signals in Anterior Cingulate Cortex

Daniel W. Bryden, Emily E. Johnson, Steven C. Tobia, Vadim Kashtelyan and Matthew R. Roesch
Journal of Neuroscience 14 December 2011, 31 (50) 18266-18274; DOI: https://doi.org/10.1523/JNEUROSCI.4715-11.2011
Daniel W. Bryden
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Emily E. Johnson
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Steven C. Tobia
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Vadim Kashtelyan
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Matthew R. Roesch
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    Figure 1.

    Task, behavior, and recording sites. a, The sequence of events in each trial block. At the beginning of each recording session, one well was arbitrarily designated as short (a short 500 ms delay before reward) and the other was designated as long (a relatively long 1–7 s delay before reward) (Block 1). After the first block of trials (∼60 trials), the wells unexpectedly reversed reward contingencies (Block 2). With the transition to block 3, the delays to reward were held constant across wells (500 ms), but the size of the reward was manipulated. The well designated as long during the previous block now offered two fluid boli, whereas the opposite well offered one bolus. The reward stipulations again reversed in block 4. b, The impact of delay length (left) and reward size (right) manipulations on choice behavior during free-choice trials. c, Behavioral reflections of value comparing percentage correct on forced-choice trials for short versus long delay (left) and big versus small reward (right). d, Reaction times (odor offset to nose unpoke from odor port) on forced-choice trials (expressed in milliseconds) comparing short- versus long-delay trials and big- versus small-reward trials. e, Light-on latency measurements (house light on to nose poke in odor port) comparing the first 10 trials versus the last 10 trials per block for upshifts (2sh, 3bg, and 4bg) and downshifts (2lo and 4sm). Sh, Short; bg, big; lo, long; sm, small. f, Location of recording sites. Gray dots mark the final electrode position and gray boxes mark the locations of recording sites. Asterisks indicate planned comparisons revealing statistically significant differences (t test, p < 0.05). Error bars indicate SEMs. N = 4 rats.

  • Figure 2.
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    Figure 2.

    Single-cell example. a, b, Histogram represents firing of one neuron during the first 10 (dark gray) and last 10 (light gray) trials after upshifts and downshifts in value aligned on odor onset. c, Heat plot shows the average firing, of the same neuron, across shifts during the first and last 10 trials after reward contingencies change.

  • Figure 3.
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    Figure 3.

    Activity of ACC neurons fire more strongly after upshifts and downshifts and was correlated with attention. a, Average normalized neural activity for all 38 task-related neurons (odor onset to fluid well entry) comparing the first 10 trials in all blocks (early, solid black) to the last 10 trials in all blocks (late, dashed gray). b, Distribution reflecting the difference in task-related firing rate between early and late in a trial block (early − late)/(early + late) following either upshifts (top) or downshifts (bottom). Black bars represent the number of neurons that showed a significant difference between these responses (t test, p < 0.05). c, Correlation of firing rate changes between early and late trials after downshifts (y-axis) and upshifts (x-axis). d, Correlation between light-on latency (house light on until nose poke; y-axis) and firing rate (x-axis) either early or late within a block [(early − late)/(early + late)]. N = 4 rats.

  • Figure 4.
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    Figure 4.

    Activity in ACC was modulated by forced-choice errors and reward-prediction errors. a, Average activity of error-related (1 s following well entry) neurons (n = 16) during forced-choice errors (black) and correct forced-choice trials (gray). b, Distribution reflecting the difference in activity between forced-choice errors and forced-choice correct trials [(error − correct) /(error + correct)]. Black bars represent the number of neurons that showed a significant difference between these responses (t test, p < 0.05). c, Distributions compare neural activity in early trials and late trials within blocks (early − late)/(early + late) for trials after upshifts (top) and downshifts (right) for all reward-response cells (n = 15). Black bars represent the number of neurons that showed a significant difference between these responses (t test, p < 0.05). Scatter plot (center) marks the correlation between the two distributions. N = 4 rats.

  • Figure 5.
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    Figure 5.

    ACC encodes expected reward size, but not delay (n = 38). a, Curves representing population firing (aligned on odor onset) for expected big reward (thick black), small reward (thick gray), short delay (thin black), and long delay (dashed gray). The first 10 trials of each block were excluded from this analysis so that activity could be examined after learning. Note that reward delivery occurs ∼1.5 s after odor onset for short-, big-, and small-reward trials. Reward on long-delay trials occurs ∼1.5–8.5 s after odor onset, thus comparisons between long-delay trials and the other three trial types should not be made later during the trial. b, c, Distributions reflecting the difference in neural activity (100 ms after odor onset to well entry) between short and long [(short − long)/(short + long)] and big and small [(big − small)/(big + small)], respectively. Black bars represent the number of neurons that showed a significant difference between these responses (t test, p < 0.05). N = 4 rats.

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The Journal of Neuroscience: 31 (50)
Journal of Neuroscience
Vol. 31, Issue 50
14 Dec 2011
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Attention for Learning Signals in Anterior Cingulate Cortex
Daniel W. Bryden, Emily E. Johnson, Steven C. Tobia, Vadim Kashtelyan, Matthew R. Roesch
Journal of Neuroscience 14 December 2011, 31 (50) 18266-18274; DOI: 10.1523/JNEUROSCI.4715-11.2011

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Attention for Learning Signals in Anterior Cingulate Cortex
Daniel W. Bryden, Emily E. Johnson, Steven C. Tobia, Vadim Kashtelyan, Matthew R. Roesch
Journal of Neuroscience 14 December 2011, 31 (50) 18266-18274; DOI: 10.1523/JNEUROSCI.4715-11.2011
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