Distinct Properties of Long-Term Potentiation in the Dentate Gyrus along the Dorsoventral Axis: Influence of Age and Inhibition

Abstract

The hippocampus is important for spatial navigation, episodic memory and affective behaviour. Increasing evidence suggests that these multiple functions are accomplished by different segments along the dorsal-ventral (septal-temporal) axis. Long-term potentiation (LTP), the best-investigated cellular correlate of learning and memory, has distinct properties along this axis in the CA1 region, but so far, little is known about longitudinal differences in dentate gyrus (DG). Therefore, here we examined potential dorsoventral differences in DG-LTP using in vitro multi-electrode array recordings. In young mice, we found higher basal synaptic transmission in the dorsal DG, while the LTP magnitude markedly increased towards the ventral pole. Strikingly, these differences were greatly reduced in slices from middle-aged mice. Short-term plasticity, evaluated by paired-pulse ratios, was similar across groups. Recordings in the presence and absence of GABAA-receptor blocker picrotoxin suggested a higher inhibitory tone in the ventral DG of young mice, confirmed by an increased frequency of miniature inhibitory postsynaptic currents. Our findings support the view that the hippocampus contains discrete functional domains along its dorsoventral axis and demonstrate that these are subject to age-dependent changes. Since these characteristics are presumably conserved in the human hippocampus, our findings have important clinical implications for hippocampus- and age-related disorders.

Whole-Body 12C Irradiation Transiently Decreases Mouse Hippocampal Dentate Gyrus Proliferation and Immature Neuron Number, but Does Not Change New Neuron Survival Rate

“…In fact, hippocampal function varies with distance from bregma: the anterior (also called dorsal or septal) hippocampus is linked to spatial learning and memory, while the posterior (also called ventral or temporal) hippocampus is linked to mood and emotions [ 4 , 42 , 45 , 158 , 159 , 160 ]. Neurogenesis, and neurogenesis-linked function, also varies along the longitudinal axis of the hippocampus [ 42 , 44 , 161 , 162 , 163 , 164 , 165 ]. Thus, we opted to assess 12 C irradiation-induced changes throughout the whole hippocampal DG, rather than just the rostral and mid hippocampus.…”

Neuronal surface P antigen (NSPA) modulates postsynaptic NMDAR stability through ubiquitination of tyrosine phosphatase PTPMEG

“…To generate LTP in CA3-CA1 synapses, high-frequency stimulation (HFS) was used, consisting on 2 trains of 100 pulses at 100 Hz of stimuli, with an inter-train interval of 10 s [ 84 ]. LTP in MPP-DG synapses was induced by 4 trains of high-frequency stimulation at 100 Hz, 1 s in duration and 200 μs pulse width, with 5-min interval [ 85 ]. Data were collected and analyzed offline with pClamp 10 (Molecular Devices, San Jose, CA, USA).…”

Effects of endogenous and exogenous D1/D5 dopamine receptor activation on LTP in ventral and dorsal CA1 hippocampal synapses

“…LTP is a basic synaptic model of learning and memory (Martin and Morris, ) and it is typically induced at hippocampal synapses (Bliss, Collingridge, & Morris, ). The ability of hippocampal synapses for LTP, however, is not evenly distributed along the dorsoventral axis of the hippocampus (Babiec, Jami, Guglietta, Chen, & O'Dell, ; Colgin, Kubota, Jia, Rex, & Lynch, ; Grigoryan, Korkotian, & Segal, ; Kouvaros and Papatheodoropoulos, ; Maruki, Izaki, Nomura, & Yamauchi, ; Milior et al, ; Moschovos, Kostopoulos, & Papatheodoropoulos, ; Papatheodoropoulos and Kostopoulos, ; Schreurs, Sabanov, & Balschun, ). On the contrary, the difference in LTP emblematically represents the recently emerging concept of intrinsic diversification along the dorsoventral axis of the hippocampus, recently reviewed in (Papatheodoropoulos, ; Tushev and Schuman, ).…”