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Articles, Behavioral/Cognitive

Orbitofrontal Cortex Encodes Memories within Value-Based Schemas and Represents Contexts That Guide Memory Retrieval

Anja Farovik, Ryan J. Place, Sam McKenzie, Blake Porter, Catherine E. Munro and Howard Eichenbaum
Journal of Neuroscience 27 May 2015, 35 (21) 8333-8344; DOI: https://doi.org/10.1523/JNEUROSCI.0134-15.2015
Anja Farovik
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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Ryan J. Place
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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Sam McKenzie
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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Blake Porter
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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Catherine E. Munro
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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Howard Eichenbaum
Center for Memory and Brain, Boston University, Boston, Massachusetts 02215
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  • Figure 1.
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    Figure 1.

    A, Context-guided object–reward association task, in which animals had to learn to associate objects with reward or nonreward, depending on the environmental context in which they were presented. Each trial began with the animal exploring one of the two contexts for 10 s with the objects absent. Then a barrier was used to hold the animal on one side of the context while objects were placed on the other side, then the barrier was removed so that the animal could approach and sample the pots. In Context 1, Object A was rewarded and not Object B, whereas in Context 2 Object B was rewarded and not Object A. The animal had to dig in the pot that contained the digging medium associated with reward, and refrain from digging in the nonrewarded pot. B, Picture of one context with two pots that contain distinct digging media (left, multicolor gum elastic squares; right, purple beads).

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    Figure 2.

    Reconstruction of recording sites in VO and LO cortices at ∼4.20, 4.68, and 5.16 mm anterior to bregma in animals recorded from coordinates taken from Paxinos and Watson (2007). Black dots indicate the site of the tetrode tip after recording had ended. Photomicrograph depicts burn marks from tetrode tips.

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    Figure 3.

    Examples of single-cell selectivity to different task dimensions during the sampling of objects in each context. Rasters and perievent histograms depict activity patterns of example neurons during the sampling of each object (A or B) at each position (1 or 2) within each context (1 or 2). Rewarded (+), unrewarded (−). Rasters show spikes for each object-sampling event. Time 0 indicates the onset of object sampling. The histogram represents firing rate in 100 ms time bins.

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    Figure 4.

    Population analyses. A, Mean Pearson correlation coefficient (r) of population vectors (SEM across sessions). Diff, Different. “Same object” and “different object” refer to comparisons of types of events that involve the same or different object identities, respectively. Same position and different position refers to comparisons of types of events that involve the same or different object positions within a context, respectively. “Same context” and “different context” refers to comparisons of types of events that involve the same or different contexts, respectively. Note that events that are compared across contexts necessarily involve different positions; these are considered different context comparisons. The specific comparisons were as follows: 1, Same object in the same position and context (e.g., Object A events versus other Object A events in Position 1 and Context 1); 2, different objects in the same position and context (e.g., Object A vs B in Position 1 and Context 1); 3, same objects in different positions in the same context (e.g., Object A in Position 1 vs Object A in Position 2 in Context 1); 4, different objects in different positions in the same context (e.g., Object A in position 1 vs Object B in Position 2 in Context 1); 5, Same objects in different positions within different contexts (e.g., Object A in Context 1 vs Object A in Context 2); and 6, different objects in different position and in different contexts (e.g., Object A in Context 1 vs Object B in context 2). B, Dendrogram shows the organization of event dimensions in OFC ensembles during object sampling as a function of similarities of population vectors along different dimensions of events. Note the strong dissimilarity (anticorrelation) between events with opposite associated reward values, the independence of representations for different rewarded objects in different contexts, the similarity of different nonrewarded objects in different contexts, and the stronger similarity of the same events in different positions. C1, Context 1; C2, context 2; Obj, object; left, left position; right, right position.

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    Figure 5.

    A, RSA for group data from ensembles that consisted of at least 10 neurons. B, RSAs for each animal. Diff, Different. See description of conditions in Figure 4A.

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    Figure 6.

    A, Representational similarity analysis (RSA) including only events that involved the rewarded object as the first object-sampling event in a trial. B, RSA including only events that involved the rewarded object as the second object-sampling event in a trial. See description of conditions in Figure 4A. C, Dendrogram including only events that involved the rewarded object as the first object-sampling event in a trial. D, Dendrogram including only events that involved the rewarded object as the second object-sampling event in a trial. Top level, Value; middle level, object-in-context; bottom level, position. See description of levels in Figure 4B.

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    Figure 7.

    A, Activity of example neurons during context exploration. Cells 3 and 4 are examples of neurons whose firing patterns distinguished the two contexts. Rasters and perievent histograms depict neuronal activity during exploration within each context. Time 0 is when the nose of the animal passed the entered context. B, Ensemble activity during context exploration. Within context, Cross-correlations of population vectors taken between exploration events in the same context; between context, cross-correlations of population vectors taken between explorations of different contexts. ***p < 0.0001.

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    Figure 8.

    Dynamics of position and object–value coding around onset of object-sampling events. Correlation analysis was performed for 200 ms time bins starting at −3.4 s before object-sampling onset and ending at +3.4 s after object-sampling onset, and ensemble discrimination for each dimension was represented using the d′ metric (see Materials and Methods). Light shade over the first 500 ms highlights the minimum sampling duration.

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    Figure 9.

    Systematic organization of task dimensions by orbitofrontal and dorsal hippocampal neuronal populations. Dorsal hippocampus organization based on the study of McKenzie et al. (2014).

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    Table 1.

    Encoding of task dimensions by single cells

    DimensionsInclusiveExclusive
    Count%Count%
    Context6015185
    Position5414133
    Object6216133
    Object × context149387619
    Object × position481251
    Context exploration55144712
    • Encoding of task dimensions by single neurons. Number and percentage of neurons (from 394 neurons recorded) that met statistical criteria for differentiating task dimensions during object sampling, and during context exploration. In the “Inclusive” column, neurons may be counted in more than one single dimension or interaction. For context exploration, inclusive involves neurons that also differentiated task dimensions during object sampling. Each value in the “Exclusive” column had significant selectivity for only the particular dimension or interaction specified.

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The Journal of Neuroscience: 35 (21)
Journal of Neuroscience
Vol. 35, Issue 21
27 May 2015
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Orbitofrontal Cortex Encodes Memories within Value-Based Schemas and Represents Contexts That Guide Memory Retrieval
Anja Farovik, Ryan J. Place, Sam McKenzie, Blake Porter, Catherine E. Munro, Howard Eichenbaum
Journal of Neuroscience 27 May 2015, 35 (21) 8333-8344; DOI: 10.1523/JNEUROSCI.0134-15.2015

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Orbitofrontal Cortex Encodes Memories within Value-Based Schemas and Represents Contexts That Guide Memory Retrieval
Anja Farovik, Ryan J. Place, Sam McKenzie, Blake Porter, Catherine E. Munro, Howard Eichenbaum
Journal of Neuroscience 27 May 2015, 35 (21) 8333-8344; DOI: 10.1523/JNEUROSCI.0134-15.2015
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Keywords

  • context
  • memory
  • orbitofrontal cortex
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  • retrieval
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