Dendritic morphology, local circuitry, and intrinsic electrophysiology of principal neurons in the entorhinal cortex of macaque monkeys

Abstract

Little is known about the neuroanatomical or electrophysiological properties of individual neurons in the primate entorhinal cortex. We have used intracellular recording and biocytin-labeling techniques in the entorhinal slice preparation from macaque monkeys to investigate the morphology and intrinsic electrophysiology of principal neurons. These neurons have previously been studied most extensively in rats. In monkeys, layer II neurons are usually stellate cells, as in rats, but they occasionally have a pyramidal shape. They tend to discharge trains, not bursts, of action potentials, and some display subthreshold membrane potential oscillations. Layer III neurons are pyramidal, and they do not appear to display membrane potential oscillations. The distribution of dendrites and of axon collaterals suggests that neurons in layers II and III are interconnected by a network of associational fibers. Layer V and VI neurons are pyramidal and tend to discharge trains of action potentials. The distribution of dendrites and axon collaterals suggests that there is an associative network of principal neurons in layers V and VI, and they also project axon collaterals toward superficial layers. Importantly, entorhinal cortical neurons in monkeys appear to exhibit significant differences from those in rats. Morphologically, neurons in monkey entorhinal layers II and III have more primary dendrites, more dendritic branches, and greater total dendritic length than in rats. Electrophysiologically, layer II neurons in monkeys exhibit less sag, and subthreshold oscillations are less robust and slower. Some monkey layer III neurons discharge bursts of action potentials that are not found in rats. The interspecies differences revealed by this study may influence information processing and pathophysiological processes in the primate entorhinal cortex. J. Comp. Neurol. 470:317-329, 2004.

Spontaneous Bursting Activity in the Developing Entorhinal Cortex

“…This confirms previous in vitro observations showing that mEC LIII pyramidal cells of adult rats are regularly spiking neurons that do not discharge bursts of action potentials (Dickson et al, 1997;Gloveli et al, 1997;Yoshida and Alonso, 2007). However, in brain slices of macaque monkeys, it has been shown that 19% of mEC LIII neurons display intrinsic bursting (Buckmaster et al, 2004) (tested in 2 mM [Ca 2ϩ ] o ). Prolonged intrinsic bursting activity is a feature of developing but not mature rat mEC LIII neurons.…”

HCN1 Channels Control Resting and Active Integrative Properties of Stellate Cells from Layer II of the Entorhinal Cortex

“…The electrophysiological and morphological properties of stellate cells recorded from mice were similar to previous descriptions made from stellate cells in slices obtained from rats and primates Klink and Alonso, 1997;Buckmaster et al, 2004) (supplemental Fig. 1, available at www.jneurosci.org as supplemental material).…”

“…Layer II of the MEC contains two classes of neurons that project directly to the hippocampal dentate gyrus: stellate neurons and pyramidal neurons Klink and Alonso, 1997;Buckmaster et al, 2004). Stellate neurons have complex integrative properties that may enable these neurons to play unique roles in transformation of cortical representations (Alonso and Llinas, 1989;Alonso and Klink, 1993;Giocomo et al, 2007).…”

Recurrent Circuits in Layer II of Medial Entorhinal Cortex in a Model of Temporal Lobe Epilepsy

“…Analogous to loss of hilar neurons and sprouting of granule cell axons in the dentate gyrus (Nadler et al, 1980), loss of layer III neurons in the medial entorhinal cortex, which normally projects axons superficially (Köhler, 1986) and synapses with dendritic spines (Germroth et al, 1991), might trigger or permit development of aberrant recurrent excitatory synapses among layer II stellate cells. In control animals, layer II stellate cells project axon collaterals to layers I and II (Lingenhöhl and Finch, 1991;Buckmaster et al, 2004) where they might synapse with and excite neighboring stellate cells (Biella et al, 2002). Simultaneous recordings from pairs of layer II stellate cells in control rats, however, did not reveal recurrent excitatory synapses (Dhillon and Jones, 2000).…”

“…Within the entorhinal cortex, primary axons give rise to collaterals that extend long distances, spanning Ͼ1 mm, in layers I and II where stellate cell dendrites are located (Lingenhöhl and Finch, 1991;Buckmaster et al, 2004). The arborization of their axon collaterals suggests stellate cells might normally form an associative network.…”