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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

High frequency stimulation (100 Hz) at different strengths elicits LTP of differing durations at the pp-CA1 and Sc-CA1 synapses. (A) High frequency stimulation (HFS) with a weak tetanus of 100 Hz (1 burst of 100 pulses) resulted in short term potentiation at the Sc-CA1 synapse and LTP at the pp-CA1 synapse in freely behaving rats. Synaptic potentiation at pp-CA1 synapses was significantly more prolonged than potentiation at SC-CA1 synapses (ANOVA). The line with the asterisk indicates individual time-points that were determined to be significant in the pp-CA1 responses compared to the Sc-CA1 responses, using post-hoc Fisher's LSD test. (B) Strong HFS with 100 Hz (4 bursts of 100 pulses) elicited comparable potentiation at the two synapses. (C) HFS with a weak or strong tetanus of 200 Hz [3 bursts (wHFS) or 10 bursts (HFS)] resulted in LTP of differing amplitude at pp-CA1 fEPSPs from freely behaving rats. LTP elicited with 200 Hz, 10 pulses was significantly larger than LTP elicited with 200 Hz, 3 pulses (ANOVA). The line with the asterisk indicates individual time-points in the 10 pulse group that were determined to be significant from the 3 pulse group, using post-hoc Fisher's LSD test.
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Figure 5: High frequency stimulation (100 Hz) at different strengths elicits LTP of differing durations at the pp-CA1 and Sc-CA1 synapses. (A) High frequency stimulation (HFS) with a weak tetanus of 100 Hz (1 burst of 100 pulses) resulted in short term potentiation at the Sc-CA1 synapse and LTP at the pp-CA1 synapse in freely behaving rats. Synaptic potentiation at pp-CA1 synapses was significantly more prolonged than potentiation at SC-CA1 synapses (ANOVA). The line with the asterisk indicates individual time-points that were determined to be significant in the pp-CA1 responses compared to the Sc-CA1 responses, using post-hoc Fisher's LSD test. (B) Strong HFS with 100 Hz (4 bursts of 100 pulses) elicited comparable potentiation at the two synapses. (C) HFS with a weak or strong tetanus of 200 Hz [3 bursts (wHFS) or 10 bursts (HFS)] resulted in LTP of differing amplitude at pp-CA1 fEPSPs from freely behaving rats. LTP elicited with 200 Hz, 10 pulses was significantly larger than LTP elicited with 200 Hz, 3 pulses (ANOVA). The line with the asterisk indicates individual time-points in the 10 pulse group that were determined to be significant from the 3 pulse group, using post-hoc Fisher's LSD test.

Mentions: High-frequency stimulation of the perforant path to CA1 synapse with a single burst of 100 pulses at 100 Hz (0.1 ms stimulus duration) resulted in synaptic potentiation that lasted for over 4 h whereas for Sc-CA1 the same stimulation elicited potentiation that lasted ca. 90 min (p < 0.05). The strength of potentiation at the two synapses was significantly different [ANOVA, F(1, 246) = 135.72; p < 0.001, n = 6 for Sc-CA1 and n = 7 for pp-CA1, Figure 5A]. Increasing the strength of stimulation to four bursts of 100 pulses at 100 Hz induced comparable potentiation at both pp-CA1 and Sc-CA1 synapses [ANOVA, F(1, 275) = 0.19; p > 0.05, n = 6 for Sc-CA1 and n = 8 for pp-CA1; Figure 5B].


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)

High frequency stimulation (100 Hz) at different strengths elicits LTP of differing durations at the pp-CA1 and Sc-CA1 synapses. (A) High frequency stimulation (HFS) with a weak tetanus of 100 Hz (1 burst of 100 pulses) resulted in short term potentiation at the Sc-CA1 synapse and LTP at the pp-CA1 synapse in freely behaving rats. Synaptic potentiation at pp-CA1 synapses was significantly more prolonged than potentiation at SC-CA1 synapses (ANOVA). The line with the asterisk indicates individual time-points that were determined to be significant in the pp-CA1 responses compared to the Sc-CA1 responses, using post-hoc Fisher's LSD test. (B) Strong HFS with 100 Hz (4 bursts of 100 pulses) elicited comparable potentiation at the two synapses. (C) HFS with a weak or strong tetanus of 200 Hz [3 bursts (wHFS) or 10 bursts (HFS)] resulted in LTP of differing amplitude at pp-CA1 fEPSPs from freely behaving rats. LTP elicited with 200 Hz, 10 pulses was significantly larger than LTP elicited with 200 Hz, 3 pulses (ANOVA). The line with the asterisk indicates individual time-points in the 10 pulse group that were determined to be significant from the 3 pulse group, using post-hoc Fisher's LSD test.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750210&req=5

Figure 5: High frequency stimulation (100 Hz) at different strengths elicits LTP of differing durations at the pp-CA1 and Sc-CA1 synapses. (A) High frequency stimulation (HFS) with a weak tetanus of 100 Hz (1 burst of 100 pulses) resulted in short term potentiation at the Sc-CA1 synapse and LTP at the pp-CA1 synapse in freely behaving rats. Synaptic potentiation at pp-CA1 synapses was significantly more prolonged than potentiation at SC-CA1 synapses (ANOVA). The line with the asterisk indicates individual time-points that were determined to be significant in the pp-CA1 responses compared to the Sc-CA1 responses, using post-hoc Fisher's LSD test. (B) Strong HFS with 100 Hz (4 bursts of 100 pulses) elicited comparable potentiation at the two synapses. (C) HFS with a weak or strong tetanus of 200 Hz [3 bursts (wHFS) or 10 bursts (HFS)] resulted in LTP of differing amplitude at pp-CA1 fEPSPs from freely behaving rats. LTP elicited with 200 Hz, 10 pulses was significantly larger than LTP elicited with 200 Hz, 3 pulses (ANOVA). The line with the asterisk indicates individual time-points in the 10 pulse group that were determined to be significant from the 3 pulse group, using post-hoc Fisher's LSD test.
Mentions: High-frequency stimulation of the perforant path to CA1 synapse with a single burst of 100 pulses at 100 Hz (0.1 ms stimulus duration) resulted in synaptic potentiation that lasted for over 4 h whereas for Sc-CA1 the same stimulation elicited potentiation that lasted ca. 90 min (p < 0.05). The strength of potentiation at the two synapses was significantly different [ANOVA, F(1, 246) = 135.72; p < 0.001, n = 6 for Sc-CA1 and n = 7 for pp-CA1, Figure 5A]. Increasing the strength of stimulation to four bursts of 100 pulses at 100 Hz induced comparable potentiation at both pp-CA1 and Sc-CA1 synapses [ANOVA, F(1, 275) = 0.19; p > 0.05, n = 6 for Sc-CA1 and n = 8 for pp-CA1; Figure 5B].

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