Electrophysiological Properties of CA1 Pyramidal Neurons along the Longitudinal Axis of the Mouse Hippocampus

Abstract

Evidence for different physiological properties along the hippocampal longitudinal axis is emerging. Here, we examined the electrophysiological features of neurons at different dorso-ventral sites of the mouse CA1 hippocampal region. Cell position was defined with respect to longitudinal coordinates of each slice. We measured variations in neuronal excitability, subthreshold membrane properties and neurotransmitter responses along the longitudinal axis. We found that (i) pyramidal cells of the dorsal hippocampus (DH) were less excitable than those of the ventral hippocampus (VH). Resting Membrane Potential (RMP) was more hyperpolarized and somatic Input Resistance (Ri) was lower in DH compared to VH. (ii) The Paired-pulse ratio (PPR) of focally induced synaptic responses was systematically reduced from the DH to the VH; (iii) Long-term-potentiation was most pronounced in the DH and fell gradually in the intermediate hippocampus and in the VH; (iv) the frequency of miniature GABAergic events was higher in the VH than in the DH; (v) the PPR of evoked inhibitory post-synaptic current (IPSC) was higher in the DH than in the VH. These findings indicate an increased probability of both GABA and glutamate release and a reduced plasticity in the ventral compared to more dorsal regions of the hippocampus.

Towards a Circuit-Level Understanding of Hippocampal CA1 Dysfunction in Alzheimer's Disease Across Anatomical Axes

“…With regard to intrinsic excitability, targeted recordings of these different populations in vitro have also established that the most striking difference is the relative hyperexcitability of ventral compared to dorsal neurons, evident in measurements of resting membrane potential, action potential firing rate, and input resistance (Dougherty et al, 2012; Kim and Johnston, 2015; Malik et al, 2016; Milior et al, 2016). How this translates to in vivo reponses is unclear because measurements of LTP between the two areas have been conflicting (Milior et al, 2016; Malik and Johnston, 2017).…”

“…How this translates to in vivo reponses is unclear because measurements of LTP between the two areas have been conflicting (Milior et al, 2016; Malik and Johnston, 2017). Recording of similar intrinsic measures across the transverse axis of ventral CA1, another study found that proximal CA1 tends to show higher excitability but a lower frequency of bursting neurons than distal CA1 (Jarsky et a., 2008).…”

Less means more: The magnitude of synaptic plasticity along the hippocampal dorso‐ventral axis is inversely related to the expression levels of plasticity‐related neurotransmitter receptors

“…To our knowledge, synaptic plasticity in the IH of the rat has only been examined in the dentate gyrus (Kenney and Manahan‐Vaughan, ). However, in mouse hippocampal slices, the intermediate CA1 region was shown to produce LTP of intermediate magnitude between the dorsal and ventral CA1 responses that was sustained/monitored for 60 minutes (Milior et al, ).…”

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, ).…”