Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II

Abstract

1. The electroresponsive properties of neurons from layer II of the rat medial entorhinal cortex (MEC) were studied by intracellular recording under current clamp in an in vitro brain slice preparation. From a total of 184 cells that fulfilled our criteria for recording stability, two groups of projection neurons were distinguished on the basis of their intrinsic biophysical properties and morphological characteristics (demonstrated by intracellular biocytin injection; n = 34). 2. Stellate cells (SCs) were the most abundant (69%). They were highly electroresponsive, and minimal changes (1-3 mV) of membrane potential generated an active response. Subthreshold depolarizing or hyperpolarizing current pulse injection always caused the membrane potential to attain an early peak and then sag to a lower level. Depolarization-induced "sags" were larger and determined early firing in all cells. The voltage-current relationship of SCs was markedly non-linear, demonstrating robust inward rectification in the hyperpolarizing and depolarizing range. 3. SCs generated persistent rhythmic subthreshold voltage oscillations on DC depolarization positive to -60 mV. The mean frequency of the oscillations was 8.6 Hz (theta range) at a membrane potential of approximately -55 mV, at which level occasional single spiking also occurred. At slightly more positive potentials, a striking 1- to 3-Hz repetitive bursting pattern emerged. This consisted of nonadapting trains of spikes ("clusters") interspersed with subthreshold oscillations that had a mean frequency of 21.7 Hz (beta range). 4. Nonstellate cells (39%; mostly pyramidal-like) displayed time-dependent inward rectification that was less pronounced than that of SCs, and minimal depolarization-induced sags. On threshold depolarization, firing was always preceded by a slowly rising ramp depolarization and thus occurred with a long delay. Inward rectification in the depolarizing range was very pronounced. However, non-SCs did not generate persistent rhythmic subthreshold oscillatory activity or spike clusters. 5. Of the electrophysiological parameters quantified, spike threshold, spike duration, depolarizing afterpotential amplitude and apparent membrane time constant demonstrated statistically significant differences between SCs and non-SCs. 6. The repetitive hiring properties in response to square current pulses of short duration (< 500 ms) were also different between SCs and non-SCs. First, most SCs displayed a bilinear frequency-current (f-I) relationship for only the first interspike interval, whereas most non-SCs displayed a bilinear relationship for all intervals. Second, SCs had a much steeper primary f-I slope for early intervals than non-SCs. Finally, SCs displayed more pronounced and faster spike frequency adaptation than non-SCs.(ABSTRACT TRUNCATED AT 400 WORDS)

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

“…Entorhinal Layer II stellate cells show subthreshold membrane potential oscillations when depolarized near firing threshold (Alonso and Llinas, 1989;Alonso and Klink, 1993;Giocomo et al, 2007). These subthreshold oscillations can influence the timing of action potentials and network oscillations (Alonso and Garcia-Austt, 1987;Acker et al, 2003).…”

“…The oscillations appear to be due to a hyperpolarization-activated cation current known as the h-current (Dickson et al, 2000) that differs in time constant along the dorsal to ventral axis (Giocomo and Hasselmo, 2008b). In contrast to stellate cells, membrane potential oscillations do not usually appear in Layer II and III pyramidal cells (Alonso and Klink, 1993), but are observed in Layer V pyramidal cells, where they may be caused by M-current (Yoshida and Alonso, 2007;Giocomo and Hasselmo, 2008a). Membrane potential oscillations do not appear in neurons of the lateral entorhinal cortex (Tahvildari and Alonso, 2005), and grid cells do not appear in lateral entorhinal cortex (Hargreaves et al, 2005).…”

The entorhinal cortex of the Megachiroptera: a comparative study of Wahlberg’s epauletted fruit bat and the straw-coloured fruit bat

“…Stellate cells are, in the entorhinal cortex as elsewhere, considered modified pyramidal cells (Germroth et al 1989b;Germroth et al 1991;Klink and Alonso 1997a;Peters and Jones 1984) and share with them a number of electrophysiological properties (Alonso and Klink 1993;Alonso and Llinas 1989;van der Linden and Lopes da Silva 1998). However, the two cell types differ from their morphological complements in layer III (Erchova et al 2004;van der Linden and Lopes da Silva 1998), and, for example, in their modulation by cholinergic inputs also from each other (Klink and Alonso 1997b).…”

“…The specific neuronal phenotype of grid cells has not been identified. Physiological characterisation of the possible phenotypes has focused on the classical stellate and pyramidal cell (Alonso and Klink 1993). Based on morphology, our study estimates the relative contribution of neuronal phenotypes to the cell population of layer II.…”

The role of ongoing dendritic oscillations in single-neuron dynamics

“…Intrinsic subthreshold oscillations have been found in stellate cells from entorhinal cortex layer 2 [6,7], neurons from the frontal cortex [8], neurons from the amygdala complex [9,10], and pyramidal cells and interneurons from the hippocampal CA1 area [11,12]. Several ionic conductances can underlie these oscillations.…”