Research ArticleNEUROSCIENCE

Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions

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Science Advances  17 Jul 2020:
Vol. 6, no. 29, eaaz0484
DOI: 10.1126/sciadv.aaz0484
  • Fig. 1 Excitotoxic injections of N-methyl-d-aspartate produced selective hippocampal lesions.

    (Top) Left: Presurgery sagittal MRI showing intact hippocampus and injection path. Right: Postsurgery sagittal MRIs of both right (R) and left (L) hemispheres from five monkeys showing shrunken hippocampi. (Bottom) Percent estimated cell loss for each hemisphere along the anterior-posterior axis. Solid lines are group medians, shaded areas are first and third quartiles, and dotted lines are overall means for each hemisphere.

  • Fig. 2 Hippocampal damage did not affect TI performance.

    (A) Examples of a TI set with the six adjacent training pairs and the six critical internal test pairs. (B) Hippocampal damage did not impair choice of the higher ranked item on critical internal test trials; main effect of group: F1,8 = 0.73, P = 0.795; main effect of TI set: F2,16 = 0.635, P = 0.543; group × TI set: F2,16 = 0.295, P = 0.756. (C) Hippocampal damage did not affect errors to criterion on either the pre- or postlesion TI sets; main effect of group: F1,8 = 0.130, P = 0.728; group × TI set: F1,8 = 0.531, P = 0.487. (D) Hippocampal damage did not alter how monkeys solved TI tests, as measured by the SDE (accuracy: main effect of group: F1,8 = 0.049, P = 0.830; main effect of SDE: F4,32 = 56.66, P < 0.001; group × TI set: F2,16 = 3.43, P = 0.058; SDE × TI set: F8,64 = 0.99, P = 0.446; SDE × group × TI set: F8,64 = 0.63, P = 0.749; response latency: main effect of group: F1,8 = 1.254, P = 0.295; main effect of SDE: F4,32 = 20.07, P < 0.001; group × TI set: F2,16 = 2.75, P = 0.094; SDE × TI set: F8,64 = 1.18, P = 0.346; SDE × group × TI set: F8,64 = 0.84, P = 0.574). Error bars represent SEM. Stimuli images from Flickr under a Creative Commons CC BY 2.0 Generic License.

  • Fig. 3 Hippocampal damage did not reliably impair memory for temporal order.

    (A) Trial sequence showing a green start square, five study images, a retention delay, and then a test in which the monkey had to touch the image that had appeared first during study. Example symbolic distances are indicated by arrows. The depicted test shows images 5 and 2, for a symbolic distance of 2. (B) Proportion correct as a function of symbolic distance, surgical time point, and group (control = black bars and filled gray dots, hippocampal = blue bars and open blue dots). Postoperatively, monkeys showed a strong SDE (F3,24 = 84.30, P < 0.001) but there was no difference between the groups in overall accuracy (t8 = 0.67, P = 0.520), no interaction of symbolic distance and group (F3,24 = 0.50, P = 0.689), and no group difference at any individual symbolic distance (all t8 < 1.15, all P > 0.284). Bars represent group means, each dot represents one monkey, and dots are jittered to allow visualization of individual performance. Chance is 0.5. Compare figure 2 of (7). Stimuli images from Flickr under a Creative Commons CC BY 2.0 Generic License.

  • Fig. 4 Hippocampal lesions did not impair SC.

    (A) Four example five-item lists and how one list might appear on the screen at test. The yellow arrows indicate the order in which the monkeys had to touch the images to earn food; these arrows were not shown to the monkeys. (B) Example two-image probe tests showing a within-list test at an SD of 1 and a between-list test at an SD of 2. The yellow arrow on the example screen shows the order in which the monkeys had to touch the images to earn food and was not visible during test. (C) Proportion correct on within-list probe tests as a function of SD, group, and experimental time point. Monkeys with hippocampal damage did not perform less accurately than controls overall (t8 = −0.833, P = 0.429) or at any individual SD (all t8 < 0.54, all P > 0.603). All monkeys showed a robust SDE (F3,24 = 25.303, P < 0.001), but there was no main effect of lesion group or interaction of group with any factor (all P > 0.05). Bars represent group means, and dots represent individual monkeys jittered along the x axis to help visualize individual performance. (D) As in (C) but for between-list tests. All monkeys showed a robust SDE (F1.549,12.390 = 19.626, P < 0.001), but there was no main effect of group or interaction of group with any factor (all P > 0.05). Stimuli images from Flickr under a Creative Commons CC BY 2.0 Generic License.

  • Fig. 5 Hippocampal damage did not impair shape recall.

    (Left) A monkey reproduces a three-block shape from memory after a retention interval. (Right) Hippocampal damage did not impair reproduction of two-block shapes (t8 = 0.16, P = 0.88), three-block shapes (t8 = 1.52, P = 0.17), or three-block shapes with a distractor task during the retention interval to interfere with working memory (t7 = 0.05, P = 0.96). Dotted lines represent chance in the different conditions. Dots represent individual monkeys and are jittered along the x axis to help visualize individual performance. Photo credit: Benjamin M. Basile, Emory University.

  • Fig. 6 Selective hippocampal damage did not change the pattern of false alarms during item recognition.

    (A) Error rates for control monkeys (solid black shapes) and monkeys with selective hippocampal damage (open blue shapes) as a function of error type (triangles = misses, circles = false alarms) and response latency. Hippocampal damage did not alter the classic pattern of U-shaped false alarms associated with quick but vague familiarity (main effect of response speed: F9,80 = 3.09, P = 0.003; main effect of group: F1,9 = 0.51, P = 0.475; interaction: F9,80 = 0.15, P = 0.999). Dots represent group means (±SEM) within each bin, and each bin contains 10% of trials. (B) Groups did not differ in overall recognition accuracy (pre: t8 = 0.02, P = 0.982; post: t8 = 0.59, P = 0.592). Bars represent group means (±SEM) and chance is 0. (C) Hippocampal damage did not affect the increase in false alarm rate due to addition of a response deadline (t8 = 0.33, P = 0.748). Dots represent individual monkeys, and lines represent group means. (D) False alarm rate as a function of trial type (normal nonmatch trial or probe nonmatch trial with recently seen lure) and retention interval (4 or 20 s). Monkeys showed elevated false alarms to recently seen lures (short delay: t9 = 10.30, P < 0.001; long delay: t9 = 86.33, P < 0.001), and this effect was greater with a longer retention interval (t9 = 7.21, P < 0.001), but it was not affected by selective hippocampal damage (short delay: t8 = 0.18, P = 0.858; long delay: t8 = 0.38, P = 0.716). Lines represent group means, each dot represents one monkey, and dots are jittered along the x axis to allow better visualization of individual performance.

  • Table 1 Cognitive tests used to assess hippocampal (HP) function.

    TestCognitive facultyBehavioral demonstrationRelevant HP citation(s)Prediction
    Transitive inferenceRelational representations(25)(39); (40)Impaired
    Temporal orderOne-trial order memory(1)(7)Impaired
    Simultaneous chainingHabitual order memory(27); (46)(46)Impaired 2-item probes
    Shape recallItem recollection(28)(6)Impaired
    Item recognitionFamiliarity/recollection(32)(2); (22)Altered false alarms
    Serial position curveTransfer to long-term
    memory
    (30)(24); (70)Spared
    Source memoryRecollection of study details(29)(4); (52)Impaired
    Image classificationVisual perception,
    generalization,
    discrimination
    (31)(53)Spared

Supplementary Materials

  • Supplementary Materials

    Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions

    Benjamin M. Basile, Victoria L. Templer, Regina Paxton Gazes, Robert R. Hampton

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