Prominent differences in sharp waves, ripples and complex spike bursts between the dorsal and the ventral rat hippocampus

Kouvaros, Stylianos; Papatheodoropoulos, Costas

doi:10.1016/j.neuroscience.2017.03.050

Cited by 21 publications

(24 citation statements)

References 112 publications

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“…At this time spontaneous activity was detected in the great majority of VH slices (n=56/67) but in only two DH slices (n=2/52). This is in keeping with previous studies that have shown that ventral but not dorsal transverse hippocampal slices have an increased ability to spontaneously generate SPWs under normal in vitro conditions (Papatheodoropoulos and Kostopoulos 2002;Kouvaros and Papatheodoropoulos 2017;Colgin et al 2004;Caliskan et al 2016). Actually, SPWs can be generated in a small fraction of DH slices as shown by assessment of a large population of slices in a recent study (Kouvaros and Papatheodoropoulos 2017).…”

Section: In Vitro Development Of Sharp Waves (Spws) In Ventral Hippocsupporting

confidence: 91%

“…Spontaneous field potentials consisted of synchronous events with a prominent positive phase of relatively small amplitude (25-250 μV), (Wu et al 2002;Papatheodoropoulos and Kostopoulos 2002). Previous studies have demonstrated that these spontaneous events represents an in vitro model of hippocampal sharp waves (SPWs), (Maier et al 2003;Kubota et al 2003), and this activity is regularly observed in transverse slices prepared mainly from the ventral but not the dorsal hippocampus (Kouvaros and Papatheodoropoulos 2017;Papatheodoropoulos and Kostopoulos 2002;Colgin et al 2004;Caliskan et al 2016). Because the amplitude of SPWs was fairly small especially at the beginning of their emergence, thus, to make feasible their detection original records were down sampled (at 2 kHz) and low-pass filtered at 40 Hz before the detection procedure was applied.…”

Section: Electrophysiological In Vitro Recordingsmentioning

confidence: 99%

“…Because SPWs are self organized in the denervated hippocampus (Buzsaki et al 1987) and in isolated hippocampal preparations under normal in vitro conditions (Maier et al 2003;Colgin et al 2004;Kubota et al 2003;Wu et al 2002;Aivar et al 2014;Mizunuma et al 2014;Papatheodoropoulos and Kostopoulos 2002), they are considered an endogenous hippocampus activity pattern, which however occurs with vastly higher probability in VH than in DH preparations (Papatheodoropoulos and Kostopoulos 2002;Kouvaros and Papatheodoropoulos 2017;Colgin et al 2004;Caliskan et al 2016). Although the mechanisms that underlie the physiological triggering of SPW, either in vivo or in vitro, are not known, it has been previously postulated (Buzsaki 1989(Buzsaki , 1996 and more recently indirectly corroborated by experimental evidence (Mizunuma et al 2014) that SPWs may arise from plasticity-related synaptic reorganization.…”

Section: Introductionmentioning

confidence: 99%

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Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Sotiriou

Angelatou

Papatheodoropoulos

2019

Preprint

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Molecular plasticity crucially supports adaptive cellular and network functioning in the brain. Variations in molecular plasticity may yield important differences in neuronal network dynamics between discrete brain subregions. In the present study we show that the gradual development of sharp waves (SPWs), a spontaneous network activity that is organized under normal in vitro conditions in the CA1 field of ventral but not dorsal hippocampal slices, is associated with region selective molecular reorganization. In particular, increased levels of mRNAs for specific GABA A receptor subunits (α1, β2, γ2) occurred in ventral hippocampal CA1 field during the development of SPWs. These mRNA changes were followed by a clear increase in GABA A receptor number in ventral hippocampus, as shown by [ 3 H]muscimol binding. An increase in mRNAs was also observed in dorsal slices for α2 and α5 subunits, not followed by quantitative GABA A receptor changes. Furthermore, full development of SPWs in the CA1 field (at 3 hours of slice maintenance in vitro) was followed by increased expression of immediate early genes c-fos and zif-268 in ventral hippocampal slices (measured at 5 hours in vitro). No change in c-fos and zif-268 levels is observed in the CA1 field of dorsal slices, which do not develop spontaneous activity. These results suggest that generation of SPWs could trigger specific molecular reorganization in the VH that may be related to the functional roles of SPWs. Correspondingly, the revealed increased potentiality of the ventral hippocampus for molecular reorganization may provide a clue to mechanisms that underlie the regulated emergence of SPWs along the longitudinal axis of the hippocampus. Furthermore, the present evidence suggests that dynamic tuning between spontaneous neuronal activity and molecular organization may importantly contribute to the functional segregation/heterogeneity seen along the hippocampus.

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Section: In Vitro Development Of Sharp Waves (Spws) In Ventral Hippocsupporting

confidence: 91%

Section: Electrophysiological In Vitro Recordingsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Sotiriou

Angelatou

Papatheodoropoulos

2019

Preprint

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“…Accordingly, the local ventral hippocampus circuitry with the increased sensitivity of its depressing synapses could be a favorable site of SWRs initiation. Indeed, in vitro SWRs are generated most likely in the ventral than in the dorsal hippocampus [ 74 , 75 ].…”

Section: Discussionmentioning

confidence: 99%

A gradient of frequency-dependent synaptic properties along the longitudinal hippocampal axis

et al. 2017

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BackgroundThe hippocampus is a functionally heterogeneous brain structure and specializations of the intrinsic neuronal network may crucially support the functional segregation along the longitudinal axis of the hippocampus. Short-term synaptic plasticity plays fundamental roles in information processing and may be importantly involved in diversifying the properties of local neuronal network along the hippocampus long axis. Therefore, we aimed to examine the properties of the cornu ammonis 1 (CA1) synapses along the entire dorsoventral axis of the rat hippocampus using field excitatory postsynaptic potentials from transverse rat hippocampal slices and a frequency stimulation paradigm.ResultsApplying a ten-pulse stimulus train at frequencies from 0.1 to 100 Hz to the Schaffer collaterals we found a gradually diversified pattern of frequency-dependent synaptic effects along the dorsoventral hippocampus axis. The first conditioned response was facilitated along the whole hippocampus for stimulus frequencies 10–40 Hz. However, steady-state responses or averaged responses generally ranged from maximum synaptic facilitation in the most dorsal segment of the hippocampus to maximum synaptic depression in the most ventral segment of the hippocampus. In particular, dorsal synapses facilitated for stimulus frequency up to 50 Hz while they depressed at higher frequencies (75–100 Hz). Facilitation at dorsal synapses was maximal at stimulus frequency of 20 Hz. On the contrary, the most ventral synapses showed depression regardless of the stimulus frequency, only displaying a transient facilitation at the beginning of 10–50 Hz stimulation. Importantly, the synapses in the medial hippocampus displayed a transitory behavior. Finally, as a whole the hippocampal synapses maximally facilitated at 20 Hz and increasingly depressed at 50–100 Hz.ConclusionThe short-term synaptic dynamics change gradually along the hippocampal long axis in a frequency-dependent fashion conveying distinct properties of information processing to successive segments of the structure, thereby crucially supporting functional segregation along the dorsoventral axis of the hippocampus.

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“…2B). In the dorsal hippocampus, the 30 s train stimulation lengthened the oxidative dip resulting in a 18 [12,22] These results show that ventral CA1 is more active in terms of metabolism. During the first seconds of the stimulation, cells in ventral CA1 mobilize oxidative phosphorylation more than in dorsal CA1 (the initial dip is larger), and then switch to glycolysis (from the overshoot to the peak).…”

Section: Metabolic Imaging Reveals Dorso-ventral Differencesmentioning

confidence: 65%

Spatio-temporal heterogeneity in hippocampal metabolism in control and epilepsy conditions

Brancati

Rawas

Ghestem

et al. 2020

Preprint

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Energy production, mostly via glycolysis and oxidative phosphorylation, which is at the core of cell function, varies in a circadian manner. Whether energy production is tailored to the functional needs of the networks remains poorly understood. The dorsal and ventral part of the hippocampus are involved in different functional circuits. Using metabolic imaging and metabolite sensing, we show that the ventral hippocampus favors aerobic glycolysis over oxidative phosphorylation as compared to the dorsal part in the morning. However, in the afternoon, aerobic glycolysis is decreased and oxidative phosphorylation increased in the ventral hippocampus. In the dorsal hippocampus, the metabolic activity varies less between these two times but is still weaker than in the ventral. Thus, energy metabolism is different in space (along the dorso-ventral axis) and time (in a circadian manner) in the hippocampus. A similar analysis in an experimental model of epilepsy revealed a large alteration of such spatio-temporal organization. In addition to a general hypometabolic state, the spatial difference disappeared in the morning, when seizure probability is low. In the afternoon, when seizure probability is high, the aerobic glycolysis was enhanced in both parts but this increase was stronger in the ventral area. We suggest that energy metabolism is tailored to the functions performed by brain networks, which vary in space and time. In pathological conditions, the alterations of these general rules may contribute to network dysfunctions. *

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Prominent differences in sharp waves, ripples and complex spike bursts between the dorsal and the ventral rat hippocampus

Cited by 21 publications

References 112 publications

Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

A gradient of frequency-dependent synaptic properties along the longitudinal hippocampal axis

Spatio-temporal heterogeneity in hippocampal metabolism in control and epilepsy conditions

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