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The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing.

Aksoy-Aksel A, Manahan-Vaughan D - Front Synaptic Neurosci (2013)

Bottom Line: We observed that field excitatory postsynaptic potentials at the pp-CA1 synapse have longer onset latencies and a shorter time-to-peak compared to the Sc-CA1 synapse.LTP (>24 h) was successfully evoked by tetanic afferent stimulation of pp-CA1 synapses.Paired-pulse responses also showed significant differences.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology, Medical Faculty, Ruhr University Bochum Bochum, Germany ; International Graduate School for Neuroscience, Ruhr University Bochum Bochum, Germany.

ABSTRACT
In terms of its sub-regional differentiation, the hippocampal CA1 region receives cortical information directly via the perforant (temporoammonic) path (pp-CA1 synapse) and indirectly via the tri-synaptic pathway where the last relay station is the Schaffer collateral-CA1 synapse (Sc-CA1 synapse). Research to date on pp-CA1 synapses has been conducted predominantly in vitro and never in awake animals, but these studies hint that information processing at this synapse might be distinct to processing at the Sc-CA1 synapse. Here, we characterized synaptic properties and synaptic plasticity at the pp-CA1 synapse of freely behaving adult rats. We observed that field excitatory postsynaptic potentials at the pp-CA1 synapse have longer onset latencies and a shorter time-to-peak compared to the Sc-CA1 synapse. LTP (>24 h) was successfully evoked by tetanic afferent stimulation of pp-CA1 synapses. Low frequency stimulation evoked synaptic depression at Sc-CA1 synapses, but did not elicit LTD at pp-CA1 synapses unless the Schaffer collateral afferents to the CA1 region had been severed. Paired-pulse responses also showed significant differences. Our data suggest that synaptic plasticity at the pp-CA1 synapse is distinct from the Sc-CA1 synapse and that this may reflect its specific role in hippocampal information processing.

No MeSH data available.


Related in: MedlinePlus

(A) Depth profile of evoked potentials as a result of perforant path stimulation. Example of typical field responses in vivo evoked by perforant path stimulation. The recordings started at the granule cell layer of the dentate gyrus (DG). The depth was decreased stepwise at 5 min intervals progressing “backwards” to the CA1 region. The distance between each representative recording was 160 μm. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 3 ms. (B) Evoked potentials at the CA1-stratum lacunosum moleculare synapse in response to Schaffer collateral and perforant path stimulation. Examples of typically evoked responses in vivo at the CA1-slm as a result of Schaffer collateral (analogs on the left) and perforant path stimulation (analogs traces on the right) at three different anterioposterior coordinates. The diagrams to the left of the analog traces represent coronal sections of hippocampal formation −3.14 mm (Top), −3.30 mm (middle), and −3.80 mm (bottom) from bregma (Paxinos and Watson, 1998). The histological examination of the recording site was depicted as a dot on the corresponding slide (Paxinos and Watson, 1998). All of the recordings were taken from freely behaving rats. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 5 ms for all traces. alv, alveus of the hippocampus; cg, cingulum; df, dorsal fornix; FC, fasciola cinereun; GrDG, granular layer of the dentate gyrus; hf, hippocampal fissure; Hil, hilus of the dentate gyrus; LMol, lacunosum moleculare layer of the hippocampus; Mol, molecular layer of the dentate gyrus; Or, oriens layer of the hippocampus; Py, pyramidal cell layer of the hippocampus; Rad, stratum radiatum of the hippocampus.
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Figure 2: (A) Depth profile of evoked potentials as a result of perforant path stimulation. Example of typical field responses in vivo evoked by perforant path stimulation. The recordings started at the granule cell layer of the dentate gyrus (DG). The depth was decreased stepwise at 5 min intervals progressing “backwards” to the CA1 region. The distance between each representative recording was 160 μm. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 3 ms. (B) Evoked potentials at the CA1-stratum lacunosum moleculare synapse in response to Schaffer collateral and perforant path stimulation. Examples of typically evoked responses in vivo at the CA1-slm as a result of Schaffer collateral (analogs on the left) and perforant path stimulation (analogs traces on the right) at three different anterioposterior coordinates. The diagrams to the left of the analog traces represent coronal sections of hippocampal formation −3.14 mm (Top), −3.30 mm (middle), and −3.80 mm (bottom) from bregma (Paxinos and Watson, 1998). The histological examination of the recording site was depicted as a dot on the corresponding slide (Paxinos and Watson, 1998). All of the recordings were taken from freely behaving rats. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 5 ms for all traces. alv, alveus of the hippocampus; cg, cingulum; df, dorsal fornix; FC, fasciola cinereun; GrDG, granular layer of the dentate gyrus; hf, hippocampal fissure; Hil, hilus of the dentate gyrus; LMol, lacunosum moleculare layer of the hippocampus; Mol, molecular layer of the dentate gyrus; Or, oriens layer of the hippocampus; Py, pyramidal cell layer of the hippocampus; Rad, stratum radiatum of the hippocampus.

Mentions: The depth profile of the evoked fEPSPs was recorded along a vertical tract starting from the granule cell layer of the DG and decreasing the depth, stepwise, with 5 min intervals up to the CA1 cell layer. This strategy (of beginning in the DG) was followed so that we could obtain a proper orientation as to the location of the electrode as we moved toward the CA1 region. The recordings were taken from a rat under anesthesia (Figure 2).


The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing.

Aksoy-Aksel A, Manahan-Vaughan D - Front Synaptic Neurosci (2013)

(A) Depth profile of evoked potentials as a result of perforant path stimulation. Example of typical field responses in vivo evoked by perforant path stimulation. The recordings started at the granule cell layer of the dentate gyrus (DG). The depth was decreased stepwise at 5 min intervals progressing “backwards” to the CA1 region. The distance between each representative recording was 160 μm. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 3 ms. (B) Evoked potentials at the CA1-stratum lacunosum moleculare synapse in response to Schaffer collateral and perforant path stimulation. Examples of typically evoked responses in vivo at the CA1-slm as a result of Schaffer collateral (analogs on the left) and perforant path stimulation (analogs traces on the right) at three different anterioposterior coordinates. The diagrams to the left of the analog traces represent coronal sections of hippocampal formation −3.14 mm (Top), −3.30 mm (middle), and −3.80 mm (bottom) from bregma (Paxinos and Watson, 1998). The histological examination of the recording site was depicted as a dot on the corresponding slide (Paxinos and Watson, 1998). All of the recordings were taken from freely behaving rats. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 5 ms for all traces. alv, alveus of the hippocampus; cg, cingulum; df, dorsal fornix; FC, fasciola cinereun; GrDG, granular layer of the dentate gyrus; hf, hippocampal fissure; Hil, hilus of the dentate gyrus; LMol, lacunosum moleculare layer of the hippocampus; Mol, molecular layer of the dentate gyrus; Or, oriens layer of the hippocampus; Py, pyramidal cell layer of the hippocampus; Rad, stratum radiatum of the hippocampus.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: (A) Depth profile of evoked potentials as a result of perforant path stimulation. Example of typical field responses in vivo evoked by perforant path stimulation. The recordings started at the granule cell layer of the dentate gyrus (DG). The depth was decreased stepwise at 5 min intervals progressing “backwards” to the CA1 region. The distance between each representative recording was 160 μm. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 3 ms. (B) Evoked potentials at the CA1-stratum lacunosum moleculare synapse in response to Schaffer collateral and perforant path stimulation. Examples of typically evoked responses in vivo at the CA1-slm as a result of Schaffer collateral (analogs on the left) and perforant path stimulation (analogs traces on the right) at three different anterioposterior coordinates. The diagrams to the left of the analog traces represent coronal sections of hippocampal formation −3.14 mm (Top), −3.30 mm (middle), and −3.80 mm (bottom) from bregma (Paxinos and Watson, 1998). The histological examination of the recording site was depicted as a dot on the corresponding slide (Paxinos and Watson, 1998). All of the recordings were taken from freely behaving rats. The stimulation intensity for all recordings was 200 μ A. Vertical scale bar: 5 mV, horizontal scale bar: 5 ms for all traces. alv, alveus of the hippocampus; cg, cingulum; df, dorsal fornix; FC, fasciola cinereun; GrDG, granular layer of the dentate gyrus; hf, hippocampal fissure; Hil, hilus of the dentate gyrus; LMol, lacunosum moleculare layer of the hippocampus; Mol, molecular layer of the dentate gyrus; Or, oriens layer of the hippocampus; Py, pyramidal cell layer of the hippocampus; Rad, stratum radiatum of the hippocampus.
Mentions: The depth profile of the evoked fEPSPs was recorded along a vertical tract starting from the granule cell layer of the DG and decreasing the depth, stepwise, with 5 min intervals up to the CA1 cell layer. This strategy (of beginning in the DG) was followed so that we could obtain a proper orientation as to the location of the electrode as we moved toward the CA1 region. The recordings were taken from a rat under anesthesia (Figure 2).

Bottom Line: We observed that field excitatory postsynaptic potentials at the pp-CA1 synapse have longer onset latencies and a shorter time-to-peak compared to the Sc-CA1 synapse.LTP (>24 h) was successfully evoked by tetanic afferent stimulation of pp-CA1 synapses.Paired-pulse responses also showed significant differences.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology, Medical Faculty, Ruhr University Bochum Bochum, Germany ; International Graduate School for Neuroscience, Ruhr University Bochum Bochum, Germany.

ABSTRACT
In terms of its sub-regional differentiation, the hippocampal CA1 region receives cortical information directly via the perforant (temporoammonic) path (pp-CA1 synapse) and indirectly via the tri-synaptic pathway where the last relay station is the Schaffer collateral-CA1 synapse (Sc-CA1 synapse). Research to date on pp-CA1 synapses has been conducted predominantly in vitro and never in awake animals, but these studies hint that information processing at this synapse might be distinct to processing at the Sc-CA1 synapse. Here, we characterized synaptic properties and synaptic plasticity at the pp-CA1 synapse of freely behaving adult rats. We observed that field excitatory postsynaptic potentials at the pp-CA1 synapse have longer onset latencies and a shorter time-to-peak compared to the Sc-CA1 synapse. LTP (>24 h) was successfully evoked by tetanic afferent stimulation of pp-CA1 synapses. Low frequency stimulation evoked synaptic depression at Sc-CA1 synapses, but did not elicit LTD at pp-CA1 synapses unless the Schaffer collateral afferents to the CA1 region had been severed. Paired-pulse responses also showed significant differences. Our data suggest that synaptic plasticity at the pp-CA1 synapse is distinct from the Sc-CA1 synapse and that this may reflect its specific role in hippocampal information processing.

No MeSH data available.


Related in: MedlinePlus