Intrinsic connectivity of the rat subiculum: I. Dendritic morphology and patterns of axonal arborization by pyramidal neurons

Abstract

The dendritic and axonal morphology of rat subicular neurons was studied in single cells labeled with Neurobiotin. Electrophysiological classification of cells as intrinsic burst firing or regular spiking neurons was correlated with morphologic patterns and cell locations. Every cell had dendritic branches that reached the outer molecular layer, with most cells having branches that reached the hippocampal fissure. All but two pyramidal cells had axon collaterals that entered the deep white matter (alveus). Branching patterns of apical dendrites varied as a function of the cell's soma location along the fissure-alveus axis of the cell layer. The first major dendritic branch point for most cells occurred at the superficial edge of the cell layer giving deep cells long primary apical dendrites and superficial cells short or absent primary apical dendrites. In contrast, basal dendritic arbors were similar across cells regardless of cell position. Apical and basal dendrites of all cells had numerous spines. Superficial and deep cells also differed in axonal collateralization. Deep cells (mostly intrinsically bursting [IB] class) had one or more ascending axon collaterals that typically remained within the region circumscribed by their apical dendrites. Superficial cells (mostly regular spiking [RS] class) tended to have axon collaterals that reached longer distances in the cell layer. Numerous varicosities and axonal extensions were present on axon collaterals in the cell layer and in the apical dendritic region, suggesting intrinsic connectivity. Axonal varicosities and extensions were found on axons that entered presubiculum, entorhinal cortex or CA1, supporting the notion that these were projection cells. Local collaterals were distinctly thinner than collaterals that would leave the subiculum, suggesting little or no myelin on local collaterals and some myelin on efferent fibers. We conclude that both IB and RS classes of subicular principal cells make synaptic contacts in and apical to the cell layer. Based on the patterns of axonal arborization, we suggest that subiculum has at least a crude columnar and laminar architecture, with ascending collaterals of deep cells forming columns and broader axonal arbors of superficial cells serving to distribute activity across multiple columns.

Grid cells and cortical representation

“…The connectivity can be extensive, such as between spiny stellate cells in layer IV of the barrel cortex, where the estimate is 24% as measured by in vitro multipatch recordings 133 , and between pyramidal cells of the visual cortex, where the connectivity may be even higher 134,135 . Similarly dense connectivity has been observed in several allocortical and allocortical-neocortical transition areas, such as the olfactory cortex 136 , the CA3 of the hippocampus [137][138][139] , the subiculum 140 , and layers III-VI of the MEC 106 . In contrast, there are very few networks with exclusive inhibitory connectivity similar to that of MEC layer II.…”

Local axon collaterals of area CA1 support spread of epileptiform discharges within CA1, but propagation is unidirectional

“…The large number of electrodes available and the fact that we can directly visualize their location on the slice results in very precisely directed electrodes, and the use of field recordings has the advantage of offering a much better picture of population behavior. We set out to define basic features of the intrinsic collateral system for the spread of population events in a cytoarchitechtonically simple structure with sparse connectivity, as we did in the adjacent subiculum (Harris and Stewart, 2001a;Harris et al, 2001). We discovered asymmetrical propagation, the basis for which is instructive in refining current circuit diagrams of the hippocampus.…”

“…Many regions that initiate seizure activity contain an abundance of burst firing neurons and the bursting cells have even been shown to be pacemaker cells [e.g., (Miles and Wong, 1983;Jensen and Yaari, 1997;Harris and Stewart, 2001a)]. The local intrinsic connectivity in each region typically shows a concentration of local collaterals nearest the cell of origin [with some variation in axonal density (Li et al, 1994); or variations dependent on cell types (Harris et al, 2001); reviewed in (Witter and Amaral, 2004;Amaral and Lavenex, 2007)]. …”

Activity-Dependent Depression of Local Excitatory Connections in the CA1 Region of Mouse Hippocampus

“…2B). This indicates that the polysynaptic EPSPs recorded in our experiments are not due to synaptic inputs onto CA1 pyramidal cells arising from the subiculum (Berger et al 1980;Commins et al 2002;Harris et al 2001;Knopp et al 2005) but are instead due to local excitatory connections between CA1 pyramidal cells. Moreover, activation of 5-HT 1B receptors with CP93129 (10 M), which selectively inhibits local excitatory synapses between CA1 pyramidal cells (Mlinar et al 2001(Mlinar et al , 2003, strongly suppressed polysynaptic EPSPs elicited by Schaffer collateral fiber stimulation (Fig.…”