Seasonal‐like plasticity of spontaneous firing rate in a songbird pre‐motor nucleus

Abstract

Many animals exhibit seasonal changes in behavior and its underlying neural substrates. In seasonally breeding songbirds, the brain nuclei that control song learning and production undergo substantial structural changes at the onset of each breeding season, in association with changes in song behavior. These changes are largely mediated by photoperiod-dependent changes in circulating concentrations of gonadal steroid hormones. Little is known, however, about whether changes in the electrophysiological activity of neurons accompany the dramatic morphological changes in the song nuclei. Here we induced seasonal-like changes in the song systems of adult white-crowned sparrows and used extracellular recording in acute brain slices from those individuals to study physiological properties of neurons in the robust nucleus of the arcopallium (RA), a pre-motor nucleus necessary for song production. We report that: RA neurons from birds in breeding condition show a more than twofold increase in spontaneous firing rate compared to those from nonbreeding condition; this change appears to require both androgenic and estrogenic actions; and this change is intrinsic to the RA neurons. Thus, neurons in the song circuit exhibit both morphological and physiological adult seasonal plasticity.

Seasonal-like growth and regression of the avian song control system: Neural and behavioral plasticity in adult male Gambel’s white-crowned sparrows

“…In canaries, systemic exposure to either DHT or E2 for eleven days does not increase song control nuclei volume or song rate, unlike T, which does increase HVC volume and song rate (Sartor et al, 2005). Systemic exposure to both an aromatizable androgen and an estrogen, however, produce full growth of song nuclei volumes and maximal song rate (Tramontin et al, 2003), RA soma area, and RA spontaneous firing rate (Park et al, 2005;Meitzen et al, 2007a). Exposure to the aromatase inhibitor ATD blocks the increase in RA soma area and spontaneous firing rate induced by LD photoperiod and systemic T (Meitzen et al, 2007a).…”

“…This acceleration can be blocked by systemic exposure to 1-4-6-androstatrien-3,17-dione (ATD), an aromatase inhibitor; aromatase is the enzyme that converts T into its estrogenic metabolite E2 (Meitzen et al, 2007a). Conversely, exposure to systemic E2 accelerates the increase of spontaneous firing rates and soma size in SD photoperiod and systemic T or DHT treated-birds (Park et al, 2005;Meitzen et al, 2007a). These results suggest that photoperiod might regulate aromatase expression or activity.…”

“…These metabolites have been implicated in song control system growth. In white-crowned sparrows, systemic exposure to either DHT (a nonaromatizable androgen) or E2 alone for 21 days results in substantial growth of song control nuclei (Tramontin et al, 2003), but not RA spontaneous firing rate or soma area (Park et al, 2005;Meitzen et al, 2007a). In canaries, systemic exposure to either DHT or E2 for eleven days does not increase song control nuclei volume or song rate, unlike T, which does increase HVC volume and song rate (Sartor et al, 2005).…”

“…Gambel's white-crowned sparrows are long-distance migrants that winter along the west coast and western interior of the contiguous United States, and breed in Alaska and Canada, unlike some other white-crowned sparrow subspecies such as the non-migratory Nuttall's (Farner and Lewis, 1973;Chilton et al, 1995). In the spring, longer day lengths induce an increase in plasma testosterone (T) level, which in turn triggers anatomical and electrophysiological changes in the nuclei of the song control system and in white-crowned sparrow song behavior, most notably increases in song rate, song stereotypy, and duration (Nottebohm et al, 1981;Smith et al, 1995;Brenowitz, 2004;Park et al, 2005;Meitzen et al, 2007a). The volumes of the song control nuclei HVC, Area X, and RA all increase, and the cellular mechanisms underlying these increases vary by nucleus.…”

“…In addition, we remove the subcutaneous T pellet and castrate the birds, to insure rapid and synchronous withdrawal of circulating sex steroids. This "seasonal-like" plasticity provides controlled conditions under which proximate mechanisms underlying changes in behavior and morphology can be carefully studied, which then informs field studies of non-captive animals (i.e., Park et al, 2005;Meitzen et al, 2007b).…”