Physiological Properties of Central Medial and Central Lateral Amygdala Neurons

Mounting evidence implicates the central (CE) nucleus of the amygdala in the mediation of classically conditioned fear responses. However, little data are available regarding the intrinsic membrane properties of CE amygdala neurons. Here, we characterized the physiological properties of CE medial (CE M ) and CE lateral (CE L ) amygdala neurons using whole cell recordings in brain slices maintained in vitro. Several classes of CE neurons were distinguished on the basis of their physiological properties. Most CE M cells (95%), here termed “late-firing neurons,” displayed a marked voltage- and time-dependent outward rectification in the depolarizing direction. This phenomenon was associated with a conspicuous delay between the onset of depolarizing current pulses and the first action potential. During this delay, the membrane potential ( V m ) depolarized slowly, the steepness of this depolarizing ramp increasing as the prepulse V m was hyperpolarized from −60 to −90 mV. Low extracellular concentrations of 4-aminopyridine (30 μM) reversibly abolished the outward rectification and the delay to firing. Late-firing CE M neurons displayed a continuum of repetitive firing properties with cells generating single spikes at one pole and high-frequency (≥90 Hz) spike bursts at the other. In contrast, only 56% of CE L cells displayed the late-firing behavior prevalent among CE M neurons. Moreover, these CE L neurons only generated single spikes in response to membrane depolarization. A second major class of CE L cells (38%) lacked the characteristic delay to firing observed in CE M cells, generated single spikes in response to membrane depolarization, and displayed various degrees of inward rectification in the hyperpolarizing direction. In both regions of the CE nucleus, two additional cell types were encountered infrequently (≤ 6% of our samples). One type of neurons, termed “low-threshold bursting cells” had a behavior reminiscent of thalamocortical neurons. The second type of cells, called “fast-spiking cells,” generated brief action potentials at high rates with little spike frequency adaptation in response to depolarizing current pulses. These findings indicate that the CE nucleus contains several types of neurons endowed with distinct physiological properties. Moreover, these various cell types are not distributed uniformly in the medial and lateral sector of the CE nucleus. This heterogeneity parallels anatomic data indicating that these subnuclei are part of different circuits.