- Research article
- Open Access
Higher intrinsic network excitability in ventral compared with the dorsal hippocampus is controlled less effectively by GABAB receptors
© Papatheodoropoulos. 2015
Received: 3 August 2015
Accepted: 4 November 2015
Published: 10 November 2015
Elucidating specializations of the intrinsic neuronal network between the dorsal and the ventral hippocampus is a recently emerging area of research that is expected to help us understand the mechanisms underlying large scale functional diversification along the hippocampus. The aim of this study was to characterize spontaneous network activity between the dorsal and the ventral hippocampus induced under conditions of partial or complete blockade of GABAergic inhibition (i.e. disinhibition).
Using field recordings from the CA3 and CA1 fields of hippocampal slices from adult rats I found that ventral compared with dorsal hippocampus slices displayed higher propensity for and higher frequency of occurrence of spontaneous field potentials (spfps) at every level of disinhibition. Also NMDA receptor-depended spfps (spfps-nmda) occurred with higher probability more frequently and were larger in the ventral compared with the dorsal hippocampus. Importantly, blockade of GABAB receptors produced a stronger effect in enhancing the probability of generation of spfps and spfps-nmda in the dorsal compared with the ventral hippocampal slices and increased spfps-nmda only in dorsal slices.
These results demonstrate a higher intrinsic neuronal excitability of the ventral compared with the dorsal local circuitry with the considerable contribution of NMDA receptors. Furthermore, the GABAB receptors control the total and the NMDA receptor-dependent excitation much less effectively in the ventral part of the hippocampus. It is proposed that NMDA and GABAB receptors significantly contribute to differentiate local network dynamics between the dorsal and the ventral hippocampus with important implications in the information processing performed along the long hippocampal axis.
Local neuronal networks participate to brain functions by changing their excitability status through a dynamic modulation of the balance between excitation and inhibition . The intrinsic hippocampal circuitry has been perceived as a model to understand the interactions between the various components that control the excitation/inhibition balance in local circuitry. Continuous experimental work for decades has accumulated a great amount of information about the function of intrinsic neuronal circuitry of the hippocampus . The internal circuitry of the hippocampus presents some very notable regularity, in that its fundamental structural organization is consisted of a local “trisynaptic” circuitry repeated along the long (dorsoventral or septotemporal) axis of the structure as a regular unit . The longitudinal repetition of this “canonical module” has created the persistent view of the hippocampus as a structure with homogeneity along its dorsoventral course. For long time the idea of this dorsoventral internal homogeneity of the hippocampal circuitry has neglected early neurochemical and physiological evidence showing differences along the hippocampus [4–10]. Only recently the differences along the dorsoventral axis and especially between the DH and VH have been more systematically attracted the attention of researchers. For instance, differences between DH and VH have been revealed in the synaptic transmission and neurotransmitter receptors [11–14] as well as in the synaptic plasticity [15–18]. Yet, the first characteristic difference that was observed between the two hippocampal poles was the higher susceptibility of the ventral hippocampus in rodents and the anterior hippocampus in human to epileptic activities [19, 20]. These early observations were repeatedly confirmed and extended by subsequent more thorough in vivo and in vitro studies performed in rats [4, 7, 21–30]. These studies led to the idea of the greater overall excitability of VH compared with DH. However, the mechanisms of apparent higher excitability of VH are still not well understood, perhaps because differences in network excitability arise from a combination of molecular, cellular and network mechanisms. GABAergic synaptic transmission constitutes a basic determinant of the local neuronal network excitability . A typical experimental approach to study synchronous network activity is based on the induction of spontaneous activity in isolated brain preparations . Classically, this is achieved by changing the excitation/inhibition balance through lowering inhibitory activity using the so-called disinhibition models . Indeed, GABAergic transmission could be a crucial factor in determining the threshold for excitation of the local circuit . Paradoxically, however, the effects of blockade of GABAergic transmission on the spontaneous network activity have been never examined comparatively between DH and VH. In the present study, I comparatively examined the ability of DH and VH to spontaneously generate population activity under conditions of partial or complete disinhibition using field recordings from transverse hippocampal slices. The results show that the intrinsic neuronal network of VH compared with DH exhibits higher excitability with the NMDA receptors having a significant contribution in the higher excitability of VH. Furthermore, GABABRs play a more important role in restricting network excitability in DH than in VH.
Animals and slice preparation
Recordings, data processing and analysis
Extracellular field recordings from the CA3 or CA1 fields were made using carbon fiber electrodes (diameter 5–10 µm, Kation Scientific, or World Precision Instruments Inc., USA). Recordings started at about 1.5 h after the slices were placed in the recording chamber and they were made either from the CA3 stratum pyramidale or from the CA1 stratum radiatum, as explained in the Results’ section. Signals were acquired with a Neurolog amplifier (Digitimer Limited, UK), band-pass filtered at 0.5 Hz–2 kHz, digitized at 10 kHz and stored in a computer disk using the CED 1401-plus interface and the Signal6 or the Spike2 software (Cambridge Electronic Design, Cambridge, UK) for off-line analysis. Spontaneous field potentials (spfps) and NMDAR-mediated spontaneous field potentials (spfps-nmda) were quantified by their incidence, measured as the percentage of slices displaying spontaneous activity in the population of slices studied; the rate of their occurrence, measured as the number of events per minute. Spfps-nmda were also quantified by their area, measured as the area circumscribed by the waveform of the negative field potential and the baseline.
The following drugs were used: the antagonist of ionotropic non-NMDARs 6-Cyano-7-nitroquinoxaline-2,3-dione (CNQX), the antagonist of NMDARs 3-((R)-2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP), the non-competitive antagonist of NMDARs (5S,10R)-(+)-5-methyl-10,11-dihydro-5H-dibenzo[a,d]cyclohepten-5,10-imine maleate (MK 801), the antagonists of γ-amino-butyric acid type A receptors (GABAAR) SR 95531, the GABAAR’s channel blocker picrotoxin (PTX), the antagonist of GABABRs (3-aminopropyl)(diethoxymethyl) phosphinic acid (CGP 35348), and the agonist of adenosine A1 receptors 2-chloroadenosine (adenosine). All drugs were purchased from Tocris Cookson (UK), but PTX and adenosine were obtained from Sigma (USA). They were first dissolved in water, but CNQX was dissolved in dimethyl-sulfoxide (DMSO). The v/v concentration of DMSO at the final solution was lower than 0.05 %.
The non parametric Wilcoxon and Mann–Whitney U test were used for comparisons inside and between DH and VH groups of values, respectively. For comparison of percentages the χ2 test was also used. ANOVA was used for comparison between related multiple groups of data. Values throughout the text represent mean ± SEM; “n” and numbers into parenthesis indicate the number of slices studied.
Local network excitation is higher and less effectively controlled by GABABRs in VH compared with DH
NMDAR-depended network excitation is higher and weakly controlled by GABABRs in VH compared with DH
In similarity with spfps, the rate of spfps-nmda was a function of the precise position of slice in VH but not DH (Fig. 6c). Specifically, VH slices taken from progressively more extreme positions, toward the ventral end of the structure, displayed higher rates of spfps-nmda than slices obtained from more medial positions (ANOVA, F = 2.5, p < 0.05), (Fig. 6b). Such a correlation was not observed in DH slices (ANOVA, F = 0.87, p > 0.5).
This study shows that under blockade of GABAergic transmission the local neuronal circuitry of the hippocampus is more excitable in the ventral than its dorsal segment with the considerable participation of NMDARs. Furthermore, the relatively weaker control of excitation by GABABRs appears to play an important role in the higher proneness of the ventral hippocampus to spontaneous activation.
One well proven difference between the DH and VH neuronal network is the propensity of the later to epileptic activity [4, 7, 19–30]. A characteristic expression of the particular excitability of VH compared with the DH is the higher rate of occurrence of recurrent synchronous discharges, observed especially in the in vitro hippocampal preparations under conditions of increased potassium or decreased magnesium concentration in the extracellular medium [4, 22, 26–28]. In keeping with these observations and using for the first time the experimental model of gradually increased disinhibition it is shown that the VH compared with DH displays higher rates of spfps and spfp-nmda. In addition, in the present study the higher network excitability of VH was also expressed by the greater incidence of spfps and spfps-nmda and the larger area of spfps-nmda under intact GABABR-mediated inhibition. In particular, the present results show that the intrinsic circuitry of VH is more prone to spontaneous activation at any level of gradual reduction of GABAAR-mediated transmission.
Several mechanisms have been proposed to contribute to the higher intrinsic excitability in the VH, including the excitatory and the inhibitory synaptic actions. For instance, in the CA1 field of the VH vs DH the GABAAR-mediated transmission is lower as evidenced by the impact of inhibitory recurrent circuit on the firing of principal cells [12, 13] and the different composition of GABAARs . Furthermore, the different subunit composition of NMDARs  and their different participation in the epileptogenesis between the two hippocampal poles [27, 28] has suggested that NMDARs are functionally distinct between DH and VH. Cholinergic transmission may also play a significant role in the network excitability . Apparently, a plethora of molecular, synaptic, cellular and circuit mechanisms contribute to the different excitability of the local neuronal circuitry between DH and VH. One of the major factors contributing to increased network excitability is the relatively low effectiveness of the synaptic inhibition . The disinhibition model used in the present study presents some advantages, including the fact that neuronal excitation that lead to synchronized field potentials can be studied in isolation from the confounding mechanisms of synaptic inhibition . Hence, the higher rates of spontaneous network activation observed here under blockade of GABAergic inhibition suggest that the relative contribution of the neuronal excitation in the local neuronal circuitry is higher in the VH compared with the DH. Indeed, recent observations have shown that the pyramidal neurons of the ventral hippocampus are more excitable compared with their dorsal counterparts [48, 49].
GABABRs modulate network excitation  and especially NMDAR-depended activity [45, 46]. The fact that blockade of GABABRs increased the proportion of slices that displayed either spfps or spfps-nmda, suggests that GABABR-mediated transmission regulates the excitation threshold in the local circuitry as for example occurs in the subiculum  and control synchronous discharges . Importantly, the present results show that GABABRs effectively control the overall network excitability in DH but not VH. What is more, thought GABABRs restricted NMDAR-depended network excitation in both DH and VH, this effect was considerably stronger in DH. This is the first time that GABABRs are shown to be differently involved in regulating and controlling total and NMDAR-depended network excitability between DH and VH.
The intrinsic excitability of a local neuronal network is the expression of the balance between excitation and inhibition that dynamically tunes the function and therefore the output of a local neuronal circuit into a specific mode at any given instance. It is proposed that NMDARs and GABABRs play significant roles in sculpting this balance in DH and VH. It has been shown that partial blockade of inhibition leads to network oscillations . It is noted that spontaneous activation of the VH local network occurred even at small reductions in GABAARergic inhibition induced by small concentrations of SR 95531. Small reductions of GABAergic inhibition such as those used in the present study favor the activity of sharp wave—ripples  which is the only one physiological endogenous network activity of the hippocampus. Actually, the generation of the ripple oscillation requires an accurate balance between excitation and inhibition in the local circuitry . The higher excitability of the VH implies that physiological activation of the hippocampal network may arise from this part of the hippocampus. This should have important implications for the processing of the incoming information in the hippocampal circuitry. Indeed, the activity of sharp waves is self-organized with greater probability in ventral compared with dorsal hippocampal slices . Similarly, sharp waves first emerge in the ventral segment of the hippocampus and then spread toward its dorsal end or they remain localized in the ventral pole . It is then postulated that the higher network excitability of VH is the manifestation of the particular functional demands assigned to this part of the hippocampus.
The present results show that GABABRs and NMDARs importantly contribute to the higher intrinsic excitability of the VH compared with the DH local circuitry. The higher excitability of the VH intrinsic network may express the different way of information processing performed from the ventral compared with the dorsal segment of the hippocampus. It is hypothesized that functional specializations of basic local network parameters such as GABABRs and NMDARs support the distinct roles played by DH and VH networks. Adaptive modifications in other parameters of the neural circuitry contribute to keeping excitation/inhibition balance into the homeostatically regulated physiological range.
This research has been co-financed by the European Union (European Social Fund–ESF) and Greek national funds through the Operational Program ‘Education-and-Lifelong-Learning’ of the National Strategic Reference Framework (NSRF)—Research Funding Program: Thales. Investing in knowledge society through the European Social Fund; (# MIS: 380342).
The author declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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