Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus

Abstract

We performed patch-clamp recordings from morphologically identified and anatomically mapped pyramidal neurons of the ventral hippocampus to test the hypothesis that bursting neurons are distributed on a gradient from the CA2/CA1 border (proximal) through the subiculum (distal), with more bursting observed at distal locations. We find that the well-defined morphological boundaries between the hippocampal subregions CA1 and subiculum do not correspond to abrupt changes in electrophysiological properties. Rather, we observed that the percentage of bursting neurons is linearly correlated with position in the proximal-distal axis across the CA1 and the subiculum, the percentages of bursting neurons being 10% near the CA1-CA2 border, 24% at the CA1-subiculum border, and higher than 50% in the distal subiculum. The distribution of bursting neurons was paralleled by a gradient in afterdepolarization (ADP) amplitude. We also tested the hypothesis that there was an association between bursting and two previously described morphologically distinct groups of pyramidal neurons (twin and single apical dendrites) in the CA1 region. We found no difference in output mode between single and twin apical dendrite morphologies, which was consistent with the observation that the two morphologies were equally distributed across the transverse axis of the CA1 region. Taken together with the known organization of connections from CA3 to CA1 and CA1 to subiculum, our results indicate that bursting neurons are most likely to be connected to regular spiking neurons and vice versa.

Local generation of multineuronal spike sequences in the hippocampal CA1 region

“…An expected outcome of such a wide distribution of intrinsic properties is that the participation probability and temporal patterning of CA1 neurons during spontaneous ripples can be only partially dictated by the upstream CA3 neurons, and that the intrinsic properties bias the participation probability and sequential recruitment of neurons in response to optogenetic activation. In line with this reasoning, pyramidal neurons vary extensively in their responses to in vitro current injection (38,39). Thus, even if every neuron experienced an identical ramp of input current (from the CA3 population during spontaneous ripple events or from the light stimulus during synthetic ripples), diverse spike patterns and sequential activity would still ensue due to intrinsic neuronal/ circuit heterogeneity.…”

Hippocampal Formation

“…Bursting cells are more numerous deep in the layer, whereas regular spiking cells are more common superficially . However, it is also reported that the percentage of bursting cells is linearly correlated to the position along the proximodistal axis, with approximately 10% of bursting neurons in proximal Sub and more than 50% in distal Sub (Jarsky et al, 2008;Kim and Spruston, 2012). Both cell types may actually only reflect a single class of neurons sharing a burst mechanism that is stronger in some cells (Staff et al, 2000).…”

Differential cAMP Signaling at Hippocampal Output Synapses

“…Subicular pyramidal cells project to a variety of cortical and subcortical structures (Stewart and Wong, 1993;Amaral and Witter, 1995) and they have been shown to be differentially distributed in the proximo-to-distal and deep-to-superficial axes of the subiculum (Greene and Totterdell, 1997;Staff et al, 2000;Harris et al, 2001;Menendez de la Prida et al, 2003;Jarsky et al, 2008). Future studies will have to map the target structures of bursting and regular firing cells to unravel the physiological implications of cell-specific plasticity at hippocampal output synapses.…”