Similar Synaptic and Current Input Properties of Aromatase and Nonaromatase Neurons in the Zebra Finch Auditory Telencephalon

Abstract/SummaryEstrogens, commonly known for their role in sexual development and maturation, support a wide variety of brain functions, including cognition, neuroprotection, and sensory processing. For example, in a songbird auditory forebrain region, caudomedial nidopallium (NCM), neuroestrogens are elevated in response to conspecific vocal and social stimuli; in turn, elevated neuroestrogens in NCM are known to rapidly enhance auditory processing independent of sex. Despite the pivotal role of neuroestrogens for brain function, it remains largely unknown whether aromatase (neuroestrogen-synthesizing) neurons differ in their cellular and physiological properties from non-aromatase-expressing neurons, as might be expected from specializations seen in other steroidogenic cell types (e.g., adrenal cells). Therefore, we systematically profiled aromatase and nonaromatase expressing NCM neurons to determine how they might differ in synaptic and current input properties, using ex vivo whole-cell electrophysiology followed by immunohistochemistry to reveal aromatase expression. Current-clamp recordings revealed no differences between aromatase and nonaromatase neurons, aside from a modest divergence in the time to reach peak membrane afterhyperpolarization. Similarly, voltage-clamp recordings of post-synaptic currents revealed no significant differences between the two cell types, suggesting that they share similar synaptic input density. Therefore, aromatase and nonaromatase NCM neurons share similar intrinsic membrane properties (e.g. excitability) and synaptic input dynamics in the higher songbird pallium. Our findings leave open the possibility that diverging computational and/or modulatory roles for aromatase vs. non-aromatase neurons could be due to projection- or neurochemical-specificity in their afferents and efferents. Significance StatementNeuroestrogens, locally synthesized in the brain by aromatase-expressing neurons, modulate neural circuit function across diverse brain regions, yet it remains unclear whether these cells represent a specialized neuronal population. We used whole-cell electrophysiology and post hoc identification of recorded neurons in the zebra finch auditory forebrain to compare the intrinsic and synaptic properties of aromatase and nonaromatase neurons. Confirming and extending previous findings, we show that aromatase-expressing neurons are not defined by unique electrophysiological properties. Instead, they appear to be functionally integrated within auditory circuits, supporting an alternative idea that neuroestrogen signaling acts through flexible neuromodulatory mechanisms rather than specialized neuronal properties. These findings do not exclude the possibility that aromatase neurons receive selective modulatory input from other brain regions.