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Brief Communications

Chronic Stress Induces a Selective Decrease in AMPA Receptor-Mediated Synaptic Excitation at Hippocampal Temporoammonic-CA1 Synapses

Angy J. Kallarackal, Mark D. Kvarta, Erin Cammarata, Leelah Jaberi, Xiang Cai, Aileen M. Bailey and Scott M. Thompson
Journal of Neuroscience 2 October 2013, 33 (40) 15669-15674; DOI: https://doi.org/10.1523/JNEUROSCI.2588-13.2013
Angy J. Kallarackal
1Department of Physiology,
3Programs in Neuroscience and Membrane Biology,
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Mark D. Kvarta
1Department of Physiology,
3Programs in Neuroscience and Membrane Biology,
4Medical Scientist Training Program, University of Maryland School of Medicine, Baltimore, Maryland 21201, and
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Erin Cammarata
5Department of Psychology, Saint Mary's College of Maryland, St. Mary's City, Maryland 20686
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Leelah Jaberi
1Department of Physiology,
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Xiang Cai
1Department of Physiology,
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Aileen M. Bailey
5Department of Psychology, Saint Mary's College of Maryland, St. Mary's City, Maryland 20686
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Scott M. Thompson
1Department of Physiology,
2Department of Psychiatry,
3Programs in Neuroscience and Membrane Biology,
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    Figure 1.

    Chronic stress impairs AMPAR-mediated synaptic excitation at TA-CA1 synapses. a, fEPSPs recorded in SLM in response to stimuli delivered at a graded series of intensities in Mg2+-free saline. Each line represents a series of responses from one slice from control (black) or CUS (gray) rats. Sets of data from representative slices shown above. b, Mean of the slopes of straight line fits to the data in a in control rats (n = 6), CUS rats (n = 6), and CUS rats administered fluoxetine (n = 8) in Mg2+-free saline before (left) and after (right) addition of DNQX. c, Mean of the slope of the AMPAR-mediated and NMDAR-mediated components taken from each slice at a stimulation intensity that produced a fiber volley of ∼0.15 mV. d, TA-CA1 fEPSP slope is plotted before and after induction of LTP in slices from control (black, n = 8 slices) and CUS animals (gray, n = 11 slices). *p < 0.05, **p < 0.01.

  • Figure 2.
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    Figure 2.

    Chronic stress decreases Glu1 expression selectively. a, GluA1 expression, normalized to β-actin levels. Samples taken from SLM in slices from control rats (n = 6), CUS rats (n = 6), and CUS rats administered fluoxetine (n = 4). b, PSD-95 (n = 5 control, 6 CUS), but not GluA2 or GluN1 (n = 8,8,9) expression, was decreased in SLM in CUS tissue compared with controls. c, GluA1 expression was decreased selectively in SLM (n = 7,6) in CUS tissue compared with controls, but not in SR (n = 5,5). *p < 0.05, Mann–Whitney U test.

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    Figure 3.

    Decreases in AMPAR-mediated excitation are specific to TA-CA1 synapses and correlated with affective state. a, Mean AMPA/NMDA ratios for SC-CA1 and TA-CA1 fEPSPs in slices from control and CUS rats (synapse–group interaction, F(1,8) = 7.525, p = 0.025). There was no difference between control and CUS at SC-CA1 synapses, whereas the ratio for TA-CA1 responses was significantly different for both CUS SC-CA1 and control TA-CA1 responses. b, Sucrose preference before and after 3 weeks in control and CUS rats. The difference was significant for CUS (2 × 2 repeated-measures ANOVA group–time interaction, F(1,21) = 23.33, p = 0.0001; CUS at 3 weeks, *p < 0.05 vs all other groups, Bonferroni test). c, AMPA/NMDAR ratios for TA-CA1 and SC-CA1 responses in each slice studied are plotted against the sucrose preference of the rat from which the slices were taken. TA-CA1 responses were correlated with sucrose preference (R2 = 0.36, p = 0.025), whereas SC-CA1 responses were not (R2 = 0.003, p = 0.43).

  • Figure 4.
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    Figure 4.

    Chronic stress impairs consolidation of long-term memory. a, Comparison of the percentage of time spent in the target quadrant during an initial probe trial, after training, in a memory probe trial performed 24 h after the last training trial, and a consolidation probe trial performed 28 d after the memory trial in control (black, n = 7) and CUS (gray, n = 6) rats. There was a significant effect of time (F(3,33) = 23.96, p < 0.001) and a significant interaction (F(3,33) = 3.07, p = 0.042). Post hoc paired t tests revealed no difference between the memory and consolidation probe times in quadrant for control animals (t(5) = 0.2, p = 0.85), but a significant difference for CUS animals (t(6) = 3.44, *p = 0.014). b, There was no difference in swim speeds during the consolidation trial between control and CUS rats. c, The time in target quadrant in the consolidation trial for all animals was correlated with their sucrose preference (left, r(14) = 0.5, p = 0.072) and latency to feed in the novelty-suppressed feeding test (right, r(14) = −0.74, p = 0.002).

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The Journal of Neuroscience: 33 (40)
Journal of Neuroscience
Vol. 33, Issue 40
2 Oct 2013
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Chronic Stress Induces a Selective Decrease in AMPA Receptor-Mediated Synaptic Excitation at Hippocampal Temporoammonic-CA1 Synapses
Angy J. Kallarackal, Mark D. Kvarta, Erin Cammarata, Leelah Jaberi, Xiang Cai, Aileen M. Bailey, Scott M. Thompson
Journal of Neuroscience 2 October 2013, 33 (40) 15669-15674; DOI: 10.1523/JNEUROSCI.2588-13.2013

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Chronic Stress Induces a Selective Decrease in AMPA Receptor-Mediated Synaptic Excitation at Hippocampal Temporoammonic-CA1 Synapses
Angy J. Kallarackal, Mark D. Kvarta, Erin Cammarata, Leelah Jaberi, Xiang Cai, Aileen M. Bailey, Scott M. Thompson
Journal of Neuroscience 2 October 2013, 33 (40) 15669-15674; DOI: 10.1523/JNEUROSCI.2588-13.2013
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