Abstract
Functional diversification along the longitudinal axis of the hippocampus is a rapidly growing concept. Modulation of synaptic transmission by neurotransmitter receptors may importantly contribute to specialization of local intrinsic network function along the hippocampus. In the present study, using transverse slices from the dorsal and the ventral hippocampus of adult rats and recordings of evoked field postsynaptic excitatory potentials (fEPSPs) from the CA1 stratum radiatum, we aimed to compare modulation of synaptic transmission between the dorsal and the ventral hippocampus. We found that transient heterosynaptic depression (tHSD, <2 s), a physiologically relevant phenomenon of regulation of excitatory synaptic transmission induced by paired stimulation of two independent inputs to stratum radiatum of CA1 field, has an increased magnitude and duration in the ventral hippocampus, presumably contributing to increased input segregation in this segment of the hippocampus. GABAB receptors, GABAA receptors, adenosine A1 receptors and L-type voltage-gated calcium channels appear to contribute differently to tHSD in the two hippocampal segments; GABABRs play a predominant role in the ventral hippocampus while both GABABRs and A1Rs play important roles in the dorsal hippocampus. Activation of GABAB receptors by an exogenous agonist, baclofen, robustly and reversibly modulated both the initial fast and the late slow components of excitatory synaptic transmission, expressed by the fEPSPslope and fEPSP decay time constant (fEPSPτ), respectively. Specifically, baclofen suppressed fEPSP slope more in the ventral than in the dorsal hippocampus and enhanced fEPSPτ more in the dorsal than in the ventral hippocampus. Also, baclofen enhanced paired-pulse facilitation in the two hippocampal segments similarly. Blockade of GABAB receptors did not affect basal paired-pulse facilitation in either hippocampal segment. We propose that the revealed dorsal-ventral differences in modulation of synaptic transmission may provide a means for specialization of information processing in the local neuronal circuits, thereby significantly contributing to diversifying neuronal network functioning along the dorsal-ventral axis of hippocampus.
Highlights
Hippocampus is an elongated prototypical brain structure thought to be composed of the repetition of a basic neural circuit of excitatory synaptic connections transversely positioned to the longitudinal axis of the structure, which in rodents is extended from a septal location, dorsally, to the temporal lobe, ventrally
We examined the effects of GABAB receptor (GABABR) activation by an exogenous agonist, baclofen, and we found that baclofen suppressed the initial fast component of excitatory synaptic transmission more in the ventral than in the dorsal hippocampus and enhanced the late slow component of excitatory transmission more in the dorsal than in the ventral hippocampus
The main findings of this study are the following: (a) transient heterosynaptic depression (tHSD) induced by paired stimulation of two independent inputs to stratum radiatum of CA1 field is stronger in the ventral compared with the dorsal hippocampus; (b) Induction of tHSD depends on several mechanisms, with a predominant participation of GABABRs and A1 receptors (A1Rs) in the dorsal hippocampus and GABABRs in the ventral hippocampus; (c) Exogenous activation of GABABRs by baclofen, suppresses the initial fast component of excitatory synaptic transmission more efficiently in the ventral than in the dorsal hippocampus, and enhances the late slow component of excitatory transmission more efficiently in the dorsal than in the ventral hippocampus; (d) Exogenous, but not endogenous tonic, activation of GABABRs enhances paired-pulse facilitation (PPF) in the dorsal and the ventral hippocampus
Summary
Hippocampus is an elongated prototypical brain structure thought to be composed of the repetition of a basic neural circuit of excitatory synaptic connections transversely positioned to the longitudinal axis of the structure, which in rodents is extended from a septal location, dorsally, to the temporal lobe, ventrally. A growing body of recently acquired experimental evidence indicates that the endogenous network of the hippocampus is diversified along the long axis of the structure according to several aspects of organization, including gene expression patterns, intrinsic properties of principal cells and properties of synaptic plasticity (Papatheodoropoulos and Kostopoulos, 2000a; Maruki et al, 2001; Dong et al, 2009; Dougherty et al, 2012; Honigsperger et al, 2015; Cembrowski et al, 2016; Kouvaros and Papatheodoropoulos, 2016b; Malik et al, 2016; Milior et al, 2016; Schreurs et al, 2017; Floriou-Servou et al, 2018; ManahanVaughan, 2019); recently reviewed (Papatheodoropoulos, 2018) These data suggest that specializations in the endogenous hippocampal circuitry may fundamentally support functional segregation which is observed at a higher level of organization. The revealing of mechanisms of intrinsic network diversification along the dorsal-ventral hippocampal axis is a major challenge in the field of hippocampus research
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