Two types of intrinsic oscillations in neurons of the lateral and basolateral nuclei of the amygdala

Abstract

Intracellular recordings in the guinea pig and cat basolateral amygdaloid (BL) complex maintained as slices in vitro revealed that a subpopulation of neurons (79%) in the lateral (AL) and basolateral (ABl) nuclei generated two types of slow oscillations of the membrane potential upon steady depolarization from resting potential. The cells were of a stellate or pyramidal-like shape and possessed spiny dendrites and an axon leaving the local synaptic environment, and thus presumably represented projection neurons. Similar oscillatory activity was observed in projection neurons of the cat AL nucleus recorded in vivo. Oscillatory activity with a low threshold of activation (low-threshold oscillation, LTO) appeared as rhythmic deflections (amplitudes, 2-6 mV) of the membrane potential positive to -60 mV. Fast Fourier transformation (FFT) demonstrated a range of frequencies of LTOs between 0.5 and 9 Hz, with >80% occurring at 1-3.5 Hz and an average at 2.3 +/- 1.1 Hz. LTOs were more regular after pharmacological blockade of synaptic transmission and were blocked by tetrodotoxin (TTX). Blockade of LTOs and Na+ spikes revealed a second type of oscillatory activity (high-threshold oscillation, HTO) at depolarizations beyond -40 mV, which was capable of triggering high-threshold spikes. HTOs ranged between 1 and 7.5 Hz, with >80% occurring at 2-6 Hz and an average at 5.8 +/- 1.1 Hz. HTOs vanished at a steady membrane polarization positive to -20 mV. Current versus voltage relations obtained under voltage-clamp conditions revealed two regions of negative slope conductance at -55 to -40 mV and at around -30 mV, which largely overlapped with the voltage ranges of LTOs and HTOs. TTX abolished the first region of negative slope conductance (-55 to -40 mV) and did not significantly influence the second region of negative slope conductance. Neuronal responses to maintained depolarizing current pulses consisted of an initial high-frequency discharge (up to 100 Hz), the frequency of which depended on the amplitude of the depolarizing current pulse, followed by a progressive decline ("adaptation") toward a slow-rhythmic firing pattern. The decay in firing frequency followed a double-exponential function, with time constants averaging 57 +/- 28 ms and 3.29 +/- 1.85 s, and approached steady-state frequencies at 6.3 +/- 2.9 Hz (n = 17). Slow-rhythmic firing remained at this frequency over a wide range of membrane polarization between approximately -50 and -20 mV, although individual electrogenic events changed from Na+ spikes and underlying LTOs to high-threshold spikes and underlying HTOs. Rhythmic regular firing was only interrupted at an intermediate range of membrane polarization by the occurrence of spike doublets. In conclusion, the integrative behavior of a class of neurons in the BL complex appears to be largely shaped by the slow-oscillatory properties of the membrane. While LTOs are likely to synchronize synaptic signals near firing threshold, HTOs are a major determinant for the slow steady-state firing patterns during maintained depolarizing influence. These intrinsic oscillatory mechanisms, in turn, can be assumed to promote population activity at this particular frequency, which ranges well within that of the limbic theta (Theta) rhythm and the delta (delta) waves in the electroencephalogram during slow-wave sleep.