Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala

Key points The amygdala mediates emotional processing, in particular fear learning, and disruption of its function is thought to contribute to the developmental origins of psychiatric disorders like depression, anxiety and autism spectrum disorders. It is difficult to identify the causes of these disorders or provide effective intervention because most of what is known of amygdala physiology is based on the adult. Using the whole-cell patch clamp technique, we show that neurons in the developing rat amygdala undergo drastic changes to their electrophysiology, including passive membrane properties, intrinsic currents and resonance. This provides the first evidence that amygdala neuron physiology is dynamic before adulthood, and likely to contribute to emotional development. The results help us better understand the normative development of emotional processing and identify critical periods of maturation that may be sensitive to insult. Abstract The basolateral amygdala (BLA) is critically involved in the pathophysiology of psychiatric disorders, which often emerge during brain development. Several studies have characterized postnatal changes to the morphology and biochemistry of BLA neurons, and many more have identified sensitive periods of emotional maturation. However, it is impossible to determine how BLA development contributes to emotional development or the aetiology of psychiatric disorders because no study has characterized the physiological maturation of BLA neurons. We addressed this critical knowledge gap for the first time using whole-cell patch clamp recording in rat BLA principal neurons to measure electrophysiological properties at postnatal day (P)7, P10, P14, P21, P28 and after P35. We show that intrinsic properties of these neurons undergo significant transitions before P21 and reach maturity around P28. Specifically, we observed significant reductions in input resistance and membrane time constant of nearly 10- and 4-fold, respectively, from P7 to P28. The frequency selectivity of these neurons to input also changed significantly, with peak resonance frequency increasing from 1.0 Hz at P7 to 5.7 Hz at P28. In the same period, maximal firing frequency significantly increased and doublets and triplets of action potentials emerged. Concomitantly, individual action potentials became significantly faster, firing threshold hyperpolarized 6.7 mV, the medium AHP became faster and shallower, and a fast AHP emerged. These results demonstrate neurons of the BLA undergo vast change throughout postnatal development, and studies of emotional development and treatments for juvenile psychiatric disorders should consider the dynamic physiology of the immature BLA.