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

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.

Canonical JAK‐STAT signaling is pivotal for long‐term depression at adult hippocampal temporoammonic‐CA1 synapses

“…JAK-STAT signaling is linked to learning and memory as inhibition of JAK causes memory deficits in health (15) and in Alzheimer's disease (AD) models (16). The JAK-STAT pathway is pivotal for NMDA-LTD at hippocampal SC-CA1 synapses (17); however, it is unclear whether JAK-STAT signaling is involved in activity-dependent synaptic plasticity mechanisms at hippocampal TA-CA1 synapses, which exhibit distinct forms of plasticity (18)(19)(20)(21).…”

Involvement of intracellular Zn2+ signaling in LTP at perforant pathway–CA1 pyramidal cell synapse

“…On the basis of recent establishment of in vivo perforant pathway LTP recording (Aksoy‐Aksel & Manahan‐Vaughan, ; Gonzalez, Villarreal, Morales, & Derrick, ), the role of synaptic Zn 2+ in perforant pathway LTP was examined by our original approach, in which a recording electrode attached to a microdialysis probe was used and the recording region was locally perfused with Zn 2+ chelators in ACSF via the microdialysis probe. Perforant pathway LTP was not attenuated under perfusion with CaEDTA (10 mM), but attenuated under perfusion with ZnAF‐2DA (50 μM), suggesting that intracellular Zn 2+ signaling is required for perforant pathway LTP as well as Schaffer collateral LTP (Takeda et al, ) (Figure ).…”

Leptin Regulation of Synaptic Function at Hippocampal TA-CA1 and SC-CA1 Synapses: Implications for Health and Disease

“…Furthermore, GluA2-lacking AMPA receptors are required for the maintenance, but not induction of HFS-induced LTP at juvenile TA-CA1 synapses [59]. Recent in vivo studies demonstrate that LTP that lasts in excess of 24 h can be evoked by tetanic stimulation in freely behaving rats [56,64]. Further investigation found that this form of in vivo LTP is dependent on NMDA receptor activation [64].…”

“…The stratum radiatum contains the SC pathway which originates in the CA3 region and is the indirect input into the CA1 region. However, the temporoammonic (TA) input originates from layer III of the EC and directly innervates the stratum lacunosum-moleculare of the CA1 region [55,56]. These two inputs to CA1 neurons not only differ in receptor and ion channel composition but also in the mechanisms underlying activity-dependent synaptic plasticity evoked at these synapses [56].…”

“…However, the temporoammonic (TA) input originates from layer III of the EC and directly innervates the stratum lacunosum-moleculare of the CA1 region [55,56]. These two inputs to CA1 neurons not only differ in receptor and ion channel composition but also in the mechanisms underlying activity-dependent synaptic plasticity evoked at these synapses [56]. Indeed, the stratum lacunosum-moleculare where TA-CA1 synapses terminate, express higher levels of dopamine receptors and a larger glutamatergic NMDA component than the SC input [57,58].…”