Effect of testosterone on input received by an identified neuron type of the canary song system: a Golgi/electron microscopy/degeneration study

Abstract

Combinations of the Golgi stain, anterograde degeneration, and electron microscopy are used to further characterize the hormone-sensitive “type IV” neuron of the forebrain nucleus robustus archistriatalis (RA) of adult female canaries. Anterograde degeneration was used to “stain,” at the electron-microscopic level, the axon terminals of neurons projecting to RA from hyperstriatum ventralis, pars caudalis (HVc) and from the lateral magnocellular nucleus of the anterior neostriatum (L- MAN). The HVc neurons projecting to RA type IV cells form synapses predominantly on the dendritic spines of those cells, while L-MAN neurons that project to RA type IV cells form a 2.5:1 mixture of shaft and spine synapses. There were about 1000 synapses from HVc neurons (about 30% of all spine synapses) on typical type IV cells and about 50 synapses from L-MAN neurons. Earlier work had shown that in female canaries the dendrites of type IV neurons of the avian song control nucleus RA increase in total length after systemic testosterone treatment, and that this increase in dendritic length was accompanied by the development of malelike song. We now show that testosterone treatment also increases the number of dendritic spines present in type IV neurons. Presumably this is accompanied by an increase in the number of synaptic inputs received by type IV cells. Earlier evidence suggested that the testosterone-induced addition of extra dendritic length to type IV cells occurred at existing dendritic tips. We tested the hypothesis that these added peripheral ends received a special subset of inputs, which might then account for the change in behavior, and found it to be false. Mapping and counts of degenerating synapses resulting from lesion of HVc and L-MAN suggest that under the influence of hormone, new synapses are added throughout the dendritic tree, with no special distribution or change in ratio of inputs occurring at the tip of dendrites. Under the influence of testosterone, each type IV cell may receive only “more of the same” inputs it received before onset of treatment. We speculate on how such changes in circuitry may relate to song stability and learning.

Telencephalic Neurons Monosynaptically Link Brainstem and Forebrain Premotor Networks Necessary for Song

“…1) (Scharff and Nottebohm, 1991;Kao et al, 2005;Olveczky et al, 2005). Convergent inputs from LMAN and HVC onto RA neurons (Canady et al, 1988;Mooney, 1992) and the absence of any known direct or indirect projection from LMAN to HVC underlie the traditional view that RA is the major locus of learning-related synaptic plasticity in the song motor circuit (Doya and Sejnowski, 1998;Fiete et al, 2007). Our identification of RA HVC PNs provides a route via which LMAN could indirectly influence HVC, an arrangement that could enable the anterior forebrain pathway to modulate song premotor activity at multiple levels within the song motor circuit.…”

Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia

“…Within RA, individual neurons receive synaptic input from both HVC and LMAN (Mooney and Konishi, 1991;Stark and Perkel, 1999); these inputs are nontopographic and topographic, respectively (Johnson et al, 1995;Foster and Bottjer, 1998). However, in the adult bird, VMP synapses within RA outnumber those of the AFP (ϳ20:1) (Canady et al, 1988). B, To test the role of auditory feedback during vocal recovery after HVC microlesions, birds were deafened by bilateral cochlea removal after HVC microlesions.…”

“…1 A). Excitatory input from both HVC (VMP) and LMAN (AFP) converge onto individual RA neurons (Mooney and Konishi, 1991), although in adult birds HVC synapses in RA far outnumber those from LMAN (ϳ20:1) (Canady et al, 1988).…”

Ensemble Coding of Vocal Control in Birdsong

“…RA, in turn, projects to the hypoglossal motor nucleus with a weak myotopic organization (Vicario, 1991) and to brainstem respiratory areas (Wild, 1993). RA projection neurons also make local connections within RA (Canady et al, 1988). In contrast to the extremely sparse neuronal firing patterns in HVC, syringeal and respiratory muscles are driven by continuous control signals that contain a wide range of time scales reflecting the motif, syllable, and subsyllable acoustic structure (Goller and Suthers, 1996;Wild et al, 1998).…”