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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) Location of the drilled holes on the rat skull and electrodes. Left: the white circles indicate the position of the ground and reference screws. The black circle signifies the position of the guiding cannula that reaches the lateral ventricle. The gray circles show the planar position of (i) the recording electrode, (ii) the stimulating electrode for Schaffer collaterals and (iii) the stimulating electrode for the perforant path (angular bundle) [Modified from Paxinos and Watson (1998)]. The animals were implanted with a stimulation electrode either in the Schaffer collateral (Sc) fibers (ii) or angular bundle (iii) if not indicated otherwise. Middle: location of the recording electrode for the perforant path (pp)-CA1 synapse (black horizontal arrow). Right: tracks of a bipolar stimulating electrode at the angular bundle (small angled arrows). Middle and right: Nissl-stained hippocampal slices. (B) Histological verification of the severence of the Schaffer collateral input. Left: Nissl-stained hippocampal slices from an animal with severed Schaffer collateral input (black arrow points the recording site). Right: the corresponding drawings from the atlas for easier interpretation (Paxinos and Watson, 1998). Distance from bregma as indicated. alv, alveus of the hippocampus; df, dorsal fornix; hf, hippocampal fissure; LV, lateral ventricle. (C) fEPSP characteristics of intact and Sc-cut groups. Left: Examples of evoked potentials from intact (pp-CA1) and Sc severed (Sc-cut) animals. Vertical scale bar: 4 mV, horizontal scale bar: 5 ms. Right: Latency and time-to-peak values for the two groups (no significant difference, n = 6).
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Figure 1: (A) Location of the drilled holes on the rat skull and electrodes. Left: the white circles indicate the position of the ground and reference screws. The black circle signifies the position of the guiding cannula that reaches the lateral ventricle. The gray circles show the planar position of (i) the recording electrode, (ii) the stimulating electrode for Schaffer collaterals and (iii) the stimulating electrode for the perforant path (angular bundle) [Modified from Paxinos and Watson (1998)]. The animals were implanted with a stimulation electrode either in the Schaffer collateral (Sc) fibers (ii) or angular bundle (iii) if not indicated otherwise. Middle: location of the recording electrode for the perforant path (pp)-CA1 synapse (black horizontal arrow). Right: tracks of a bipolar stimulating electrode at the angular bundle (small angled arrows). Middle and right: Nissl-stained hippocampal slices. (B) Histological verification of the severence of the Schaffer collateral input. Left: Nissl-stained hippocampal slices from an animal with severed Schaffer collateral input (black arrow points the recording site). Right: the corresponding drawings from the atlas for easier interpretation (Paxinos and Watson, 1998). Distance from bregma as indicated. alv, alveus of the hippocampus; df, dorsal fornix; hf, hippocampal fissure; LV, lateral ventricle. (C) fEPSP characteristics of intact and Sc-cut groups. Left: Examples of evoked potentials from intact (pp-CA1) and Sc severed (Sc-cut) animals. Vertical scale bar: 4 mV, horizontal scale bar: 5 ms. Right: Latency and time-to-peak values for the two groups (no significant difference, n = 6).

Mentions: For fEPSP recordings in freely behaving rats, the animals were implanted unilaterally on the right hemisphere with a monopolar recording electrode and a bipolar stimulating electrode. For pp-CA1 and Sc-cut animals the recording electrode was positioned at the stratum lacunosum moleculare of the CA1 region (coordinates; from bregma, AP: −3.0; from midline, ML: +2.0 mm; from dura, DV: manually determined) and the stimulating electrode at the angular bundle with coordinates corresponding to the fibers of the medial perforant path (coordinates; from bregma, AP: −6.9; from midline, ML: +4.1 mm) (Figure 1A, middle and right picture, respectively). For Schaffer collateral-CA1 (Sc-CA1) animals the recording electrode was positioned at the stratum radiatum of the CA1 region (coordinates; from bregma, AP: −2.8; from midline, ML: +1.8 mm) and the stimulating electrode at the Schaffer collateral fibers (coordinates; from bregma, AP: −3.1; from midline, ML: +3.1 mm; from dura, DV: manually determined) (histology not shown) (Manahan-Vaughan and Reymann, 1995). Briefly, the dura was pierced and the electrodes were lowered slowly in the brain tissue. The evoked field excitatory postsynaptic potential (fEPSP) responses were monitored at different depths until a typical fEPSP was obtained. Except for the Sc-cut animals (described below) the electrodes were fixed with cyanoacrylate glue to the skull and the whole assembly was covered with dental cement. After surgery, the animals were placed under observation in a temperature-regulated environment. When they were fully awake and gave no signs of complications they were returned to their homecage and monitored closely for continued recovery. The wound was treated regularly with antibiotic powder. The animals were given the analgesic, meloxicam (0.2 mg/kg i.p.), to alleviate post-operative discomfort.


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) Location of the drilled holes on the rat skull and electrodes. Left: the white circles indicate the position of the ground and reference screws. The black circle signifies the position of the guiding cannula that reaches the lateral ventricle. The gray circles show the planar position of (i) the recording electrode, (ii) the stimulating electrode for Schaffer collaterals and (iii) the stimulating electrode for the perforant path (angular bundle) [Modified from Paxinos and Watson (1998)]. The animals were implanted with a stimulation electrode either in the Schaffer collateral (Sc) fibers (ii) or angular bundle (iii) if not indicated otherwise. Middle: location of the recording electrode for the perforant path (pp)-CA1 synapse (black horizontal arrow). Right: tracks of a bipolar stimulating electrode at the angular bundle (small angled arrows). Middle and right: Nissl-stained hippocampal slices. (B) Histological verification of the severence of the Schaffer collateral input. Left: Nissl-stained hippocampal slices from an animal with severed Schaffer collateral input (black arrow points the recording site). Right: the corresponding drawings from the atlas for easier interpretation (Paxinos and Watson, 1998). Distance from bregma as indicated. alv, alveus of the hippocampus; df, dorsal fornix; hf, hippocampal fissure; LV, lateral ventricle. (C) fEPSP characteristics of intact and Sc-cut groups. Left: Examples of evoked potentials from intact (pp-CA1) and Sc severed (Sc-cut) animals. Vertical scale bar: 4 mV, horizontal scale bar: 5 ms. Right: Latency and time-to-peak values for the two groups (no significant difference, n = 6).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 1: (A) Location of the drilled holes on the rat skull and electrodes. Left: the white circles indicate the position of the ground and reference screws. The black circle signifies the position of the guiding cannula that reaches the lateral ventricle. The gray circles show the planar position of (i) the recording electrode, (ii) the stimulating electrode for Schaffer collaterals and (iii) the stimulating electrode for the perforant path (angular bundle) [Modified from Paxinos and Watson (1998)]. The animals were implanted with a stimulation electrode either in the Schaffer collateral (Sc) fibers (ii) or angular bundle (iii) if not indicated otherwise. Middle: location of the recording electrode for the perforant path (pp)-CA1 synapse (black horizontal arrow). Right: tracks of a bipolar stimulating electrode at the angular bundle (small angled arrows). Middle and right: Nissl-stained hippocampal slices. (B) Histological verification of the severence of the Schaffer collateral input. Left: Nissl-stained hippocampal slices from an animal with severed Schaffer collateral input (black arrow points the recording site). Right: the corresponding drawings from the atlas for easier interpretation (Paxinos and Watson, 1998). Distance from bregma as indicated. alv, alveus of the hippocampus; df, dorsal fornix; hf, hippocampal fissure; LV, lateral ventricle. (C) fEPSP characteristics of intact and Sc-cut groups. Left: Examples of evoked potentials from intact (pp-CA1) and Sc severed (Sc-cut) animals. Vertical scale bar: 4 mV, horizontal scale bar: 5 ms. Right: Latency and time-to-peak values for the two groups (no significant difference, n = 6).
Mentions: For fEPSP recordings in freely behaving rats, the animals were implanted unilaterally on the right hemisphere with a monopolar recording electrode and a bipolar stimulating electrode. For pp-CA1 and Sc-cut animals the recording electrode was positioned at the stratum lacunosum moleculare of the CA1 region (coordinates; from bregma, AP: −3.0; from midline, ML: +2.0 mm; from dura, DV: manually determined) and the stimulating electrode at the angular bundle with coordinates corresponding to the fibers of the medial perforant path (coordinates; from bregma, AP: −6.9; from midline, ML: +4.1 mm) (Figure 1A, middle and right picture, respectively). For Schaffer collateral-CA1 (Sc-CA1) animals the recording electrode was positioned at the stratum radiatum of the CA1 region (coordinates; from bregma, AP: −2.8; from midline, ML: +1.8 mm) and the stimulating electrode at the Schaffer collateral fibers (coordinates; from bregma, AP: −3.1; from midline, ML: +3.1 mm; from dura, DV: manually determined) (histology not shown) (Manahan-Vaughan and Reymann, 1995). Briefly, the dura was pierced and the electrodes were lowered slowly in the brain tissue. The evoked field excitatory postsynaptic potential (fEPSP) responses were monitored at different depths until a typical fEPSP was obtained. Except for the Sc-cut animals (described below) the electrodes were fixed with cyanoacrylate glue to the skull and the whole assembly was covered with dental cement. After surgery, the animals were placed under observation in a temperature-regulated environment. When they were fully awake and gave no signs of complications they were returned to their homecage and monitored closely for continued recovery. The wound was treated regularly with antibiotic powder. The animals were given the analgesic, meloxicam (0.2 mg/kg i.p.), to alleviate post-operative discomfort.

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