Two types of intrinsic oscillations in neurons of the lateral and
basolateral nuclei of the amygdala.
Hans-Christian Pape , Denis Par, and Robert B. Driesang.
Institut for Physiologie, Medizinische Fakultet, Otto-von-Guericke-
Universitet, D-39120 Magdeburg, Germany, Departement de Physiologie, Faculte
de Medecine, Université Laval, Queébec G1K 7P4, Canada.
APStracts 4:213007N, 1997.
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,
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
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 upon the amplitude of the depolarizing current pulse,
followed by a progressive decline („adaptation“) towards 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
basolateral amygdaloid 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 (?) rhythm and the delta (?) waves in the
electroencephalogram (EEG) during slow-wave sleep.
Received 18 March 1997; accepted in final form 25 August 1997.
APS Manuscript Number J231-7.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 5 September 1997