Hc. Pape et al., 2 TYPES OF INTRINSIC OSCILLATIONS IN NEURONS OF THE LATERAL AND BASOLATERAL NUCLEI OF THE AMYGDALA, Journal of neurophysiology, 79(1), 1998, pp. 205-216
Intracellular recordings in the guinea pig and cat basolateral amygdal
oid (BL) complex maintained as slices in vitro revealed that a subpopu
lation of neurons (79%) in the lateral (AL) and basolateral (ABI) nucl
ei 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 repr
esented projection neurons. Similar oscillatory activity was observed
in projection neurons of the cat AL nucleus recorded in vivo. Oscillat
ory activity with a low threshold of activation (low-threshold oscilla
tion, LTO) appeared as rhythmic deflections (amplitudes, 2-6 mV) of th
e 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. LTO
s were more regular after pharmacological blockade of synaptic transmi
ssion 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 ir 1.1 Hz. HTOs
vanished at a steady membrane polarization positive to -20 mV. Current
versus voltage relations obtained under voltage-clamp conditions reve
aled two regions of negative slope conductance at -55 to -40 mV and at
around -30 mV, which largely overlapped with the voltage ranges of LT
Os and HTOs. TTX abolished the first region of negative slope conducta
nce (-55 to -40 mV) and did not significantly influence the second reg
ion of negative slope conductance. Neuronal responses to maintained de
polarizing current pulses consisted of an initial high-frequency disch
arge (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 fi
ring frequency followed a double-exponential function, with time const
ants 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 re
mained at this frequency over a wide range of membrane polarization be
tween approximately -50 and -20 mV, although individual electrogenic e
vents changed from Na+ spikes and underlying LTOs to high-threshold sp
ikes and underlying HTOs. Rhythmic regular firing was only interrupted
at an intermediate range of membrane polarization by the occurrence o
f spike doublets. In conclusion, the integrative behavior of a class o
f neurons in the BL complex appears to be largely shaped by the slow-o
scillatory properties of the membrane. While LTOs are likely to synchr
onize synaptic signals near firing threshold, HTOs are a major determi
nant for the slow steady-state firing patterns during maintained depol
arizing influence. These intrinsic oscillatory mechanisms, in turn, ca
n be assumed to promote population activity at this particular frequen
cy, which ranges well within that of the limbic theta (theta) rhythm a
nd the delta (delta) waves in the electroencephalogram during slow-wav
e sleep.