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ARTICLE

Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination

Stephan G. Anagnostaras, Stephen Maren and Michael S. Fanselow
Journal of Neuroscience 1 February 1999, 19 (3) 1106-1114; DOI: https://doi.org/10.1523/JNEUROSCI.19-03-01106.1999
Stephan G. Anagnostaras
1Department of Psychology and Brain Research Institute, University of California, Los Angeles, California 90095-1563, and
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Stephen Maren
2Department of Psychology and Neuroscience Program, University of Michigan, Ann Arbor, Michigan 48109
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Michael S. Fanselow
1Department of Psychology and Brain Research Institute, University of California, Los Angeles, California 90095-1563, and
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  • Fig. 1.
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    Fig. 1.

    Experiment 1. Sample schematic view of within-subjects procedures. The animals were given remote conditioning in one context, and 50 d later they received recent training in a different context (with a different tone), followed by dorsal hippocampal or sham lesions 1 d later. After 10 d of recovery, they were given independent freezing tests for remote and recent, context and tone fear memory. The exact contexts and test orders used were counterbalanced. Drawings are not to scale.

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    Fig. 2.

    Histological reconstruction of representative electrolytic lesion of the dorsal hippocampus.

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    Fig. 3.

    Experiment 1. Temporally graded retrograde amnesia of contextual fear: within-subjects examination. A, Remote contextual fear. Rats that received DH lesions exhibited equivalent levels of freezing (% time ± SEM, for each minute of the 8 min test) as sham animals to the remotely acquired context, for which they were trained 50 d before the lesion.B, Recent contextual fear. The very same DH-lesioned rats exhibited a severe amnesia of contextual memory that was 1 d old at the time of the lesion. C, Context summary. This is the same data as in A and B, averaged for the first 6 min of each test (6 min was used to make the levels more comparable to the tone tests; see Fig. 4). DH-lesioned rats exhibited a severe but time-limited retrograde amnesia of contextual fear.

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    Fig. 4.

    Experiment 1. Tone conditioning. For each test, the animal was placed into a novel context (C) and after a 2 min baseline (BL) period, a tone (remote or recent) played continuously for 6 min. A, Remote tone fear. DH-lesioned rats exhibited equivalent levels of freezing (% time ± SEM, for each minute of the 8 min test) as sham animals to the remotely acquired tone, for which they were trained 50 d before the lesion. B, Recent tone fear. DH-lesioned rats exhibited no deficit in freezing to the recently acquired tone, for which they were trained 1 d before the lesion. C, Tone summary. Same data as A and B, averaged for the 6 min that the tone was on. DH-lesioned rats exhibited normal levels of tone freezing.

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    Fig. 5.

    Experiment 2. Further increase in the level of context fear relative to tone fear. Rats were trained only in one training context with one tone, and then given DH lesions 1 d later. A, Recent contextual fear. DH-lesioned animals exhibited a severe deficit in context freezing (% time ± SEM, for each minute of the 8 min test), although fear levels in sham animals were nearly asymptotic. B, Recent tone fear. DH-lesioned animals did not exhibit deficits in tone freezing, even as tone fear extinguished across the test period and became weaker.C, Interaction. Same data as A andB, averaged for the first 6 min of the context test and 6 min that the tone was on test (6 min was used to make the levels more comparable). DH-lesioned animals exhibited a deficit only in contextual freezing, although tone fear was substantially weaker than context fear in Sham animals.

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    Fig. 6.

    Experiment 3. The generality of hippocampal hyperactivity. Rats were placed on a dark open field (lit only by a 25 W red bulb), and crossovers were scored for 4 min. Two bright lights (two 100 W white bulbs) were then shined onto the open field, and crossovers were scored for another 4 min. Open-field activity was assessed by scoring segment crossovers (mean ± SEM), which are depicted for each minute of the dark and light periods. DH-lesioned animals exhibited a robust hyperactivity during the dark phase of the test, but this hyperactivity disappeared when the lights were turned on. Moreover, hippocampal lesion-induced hyperactivity observed during the dark phase appeared to result from a lack of habituation that was seen in sham animals.

Tables

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    Table 1.

    Peak fear

    ContextTone
    Experiment 1
     Remote
      Sham95.8  ± 2.075.8  ± 8.2p = 0.02*
      DH96.6  ± 2.475.0  ± 11.7p = 0.2
    p > 0.6p > 0.9
     Recent
      Sham95.8  ± 1.680.0  ± 6.3p = 0.01*
      DH71.6  ± 8.471.6  ± 12.5p > 0.99
    p = 0.02*p > 0.9
    Experiment 2
      Sham99.3  ± 0.784.0  ± 7.6p = 0.03*
      DH79.7  ± 9.192.2  ± 4.7p = 0.2
    p < 0.01*p > 0.8
    • Peak freezing (mean ± SEM) was computed by taking each rat’s maximum freezing for any continuous minute during each of the 8-min context and 6-min (post-baseline) tone fear tests. Paired comparisons contrast context and tone freezing within-subjects using the Wilcoxon signed-rank post hoc; unpaired comparisons contrast Sham and DH groups for each test using the Mann–Whitney U post hoc. For both Experiments 1 and 2, DH lesions produced significant impairments in average (Figs. 3-5) and peak (above) recent context fear but not remote context or tone fear. For Sham animals, peak (above) and average (Figs. 3-5) context fear was greater than, or equivalent to, but not weaker than tone fear.

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The Journal of Neuroscience: 19 (3)
Journal of Neuroscience
Vol. 19, Issue 3
1 Feb 1999
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Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination
Stephan G. Anagnostaras, Stephen Maren, Michael S. Fanselow
Journal of Neuroscience 1 February 1999, 19 (3) 1106-1114; DOI: 10.1523/JNEUROSCI.19-03-01106.1999

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Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination
Stephan G. Anagnostaras, Stephen Maren, Michael S. Fanselow
Journal of Neuroscience 1 February 1999, 19 (3) 1106-1114; DOI: 10.1523/JNEUROSCI.19-03-01106.1999
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Keywords

  • retrograde amnesia
  • hippocampus
  • context
  • fear
  • conditioning
  • freezing
  • rat
  • activity
  • Consolidation
  • learning
  • memory

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