Dorsal-Ventral Differences in Modulation of Synaptic Transmission in the Hippocampus

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. GABA B receptors, GABA A receptors, adenosine A1 receptors and L-type voltage-gated calcium channels appear to contribute differently to tHSD in the two hippocampal segments; GABA B Rs play a predominant role in the ventral hippocampus while both GABA B Rs and A1Rs play important roles in the dorsal hippocampus. Activation of GABA B 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 (fEPSP τ ), respectively. Specifically, baclofen suppressed fEPSP slope more in the ventral than in the dorsal hippocampus and enhanced fEPSP τ more in the dorsal than in the ventral hippocampus. Also, baclofen enhanced paired-pulse facilitation in the two hippocampal segments similarly. Blockade of GABA B 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.

Extracranial 125I Seed Implantation Allows Non-invasive Stereotactic Radioablation of Hippocampal Adult Neurogenesis in Guinea Pigs

“…Different regions of the hippocampus appear to be engaged in different cognitive activities ( Shors et al, 2002 ; Bannerman et al, 2004 ; Fanselow and Dong, 2010 ; Strange et al, 2014 ; Huckleberry et al, 2018 ; Trompoukis and Papatheodoropoulos, 2020 ). It is suggested that the dorsal hippocampus may perform primarily cognitive functions, whereas the ventral part is more related to the processing of stress, emotion and affect ( Fanselow and Dong, 2010 ; Kheirbek and Hen, 2011 ).…”

The Sedentary Lifestyle and Masticatory Dysfunction: Time to Review the Contribution to Age-Associated Cognitive Decline and Astrocyte Morphotypes in the Dentate Gyrus

“…They exhibit differential rates of neurogenesis and each displays a distinct pattern of neurotransmitter receptor distribution [ 155 , 156 , 157 ]. In addition, the septal/temporal divisions of the hippocampus exhibit significant differences in behavior-induced arc gene expression [ 158 ], distinct transcriptional and epigenetic effects in response to an enriched environment or physical activity [ 82 , 159 ], and distinct pathological responses throughout aging [ 160 ]. The dorsal hippocampus is associated with spatial memory and contextual information processing, while the ventral hippocampus is related to emotional behavior in association with fear, anxiety, and reward processing [ 161 , 162 , 163 ].…”

“…Astrocyte morphology is affected by aging [ 160 , 168 , 169 , 170 , 171 , 172 ], enriched environment [ 41 , 173 ] and masticatory dysfunctions [ 27 ], in a region- and subregion-specific manner. However, our previous astrocyte analysis related to masticatory dysfunction, age and sedentary lifestyle did not explore the septal-temporal (dorsoventral) hippocampal division.…”

“…A previous report, limited to search for age influence on morphological complexity of GFAP astrocytes, demonstrated remarkable heterogeneity in the age-related changes in distinct subfields and along the dorsoventral axis of the hippocampus and in the entorhinal cortex of C57Bl6 mice [ 160 ]. These authors found that compared to 6-month-old mice the number of intersections, as a function of soma distance, increased significantly in dorsal dentate gyrus of 14-month-old mice, and the total sum of intersections, the number of processes and the total branch length followed a similar tendency, but no changes were observed in the ventral dentate gyrus.…”

Caffeine Functions by Inhibiting Dorsal and Ventral Hippocampal Adenosine 2A Receptors to Modulate Memory and Anxiety, Respectively

“…Early anatomical studies demonstrated differences between the afferent and efferent nerve projections of the dorsal hippocampus (dHPC) and ventral hippocampus (vHPC) (Swanson and Cowan, 1977). According to a current consensus, the role played by the most dorsally located hippocampal segment is on cognitive operations like spatial navigation, while internally monitoring functions related to emotionality are taken on by the ventral segment of the hippocampus (Trompoukis and Papatheodoropoulos, 2020). Moreover, some studies have found that caffeine reverts memory impairment in a depression-prone mouse strain with upregulation of adenosine A 2A receptors in the hippocampus (Machado et al, 2017), while selective A 2A R knockout in the forebrain region (striatum, hippocampus, and cortex) induces anxiety-like behavior (Wei et al, 2014).…”