Orthogonal topography in the parallel input architecture of songbird HVC

Abstract

Neural activity within the cortical premotor nucleus HVC (acronym is name) encodes the learned songs of adult male zebra finches (Taeniopygia guttata). HVC activity is driven and/or modulated by a group of five afferent nuclei (the Medial Magnocellular nucleus of the Anterior Nidopallium, MMAN; Nucleus Interface, NIf; nucleus Avalanche, Av; the Robust nucleus of the Arcopallium, RA; the Uvaeform nucleus, Uva). While earlier evidence suggested that HVC receives a uniformly distributed and nontopographic pattern of afferent input, recent evidence suggests this view is incorrect (Basista et al., ). Here, we used a double-labeling strategy (varying both the distance between and the axial orientation of dual tracer injections into HVC) to reveal a massively parallel and in some cases topographic pattern of afferent input. Afferent neurons target only one rostral or caudal location within medial or lateral HVC, and each HVC location receives convergent input from each afferent nucleus in parallel. Quantifying the distributions of single-labeled cells revealed an orthogonal topography in the organization of afferent input from MMAN and NIf, two cortical nuclei necessary for song learning. MMAN input is organized across the lateral-medial axis whereas NIf input is organized across the rostral-caudal axis. To the extent that HVC activity is influenced by afferent input during the learning, perception, or production of song, functional models of HVC activity may need revision to account for the parallel input architecture of HVC, along with the orthogonal input topography of MMAN and NIf.

Female zebra finches do not sing yet share neural pathways necessary for singing in males

“…In males, a small subpopulation of neurons in dorsal–caudal RA receives and returns connectivity with HVC (Roberts et al, ). Injecting HVC with a bidirectional tracer backfills these neurons in males, where due to the intensity of terminal labeling they are most clearly seen at portions of the dorsal–caudal margin of RA where the intensity of terminal labeling is reduced (Basista et al, ; Elliott et al, ). We did not observe a distinct population of backfilled cells at the dorsal–caudal margin of female RA, which may indicate a sex difference in RA–HVC connectivity.…”

“…Visual inspection suggests that female MMAN is not as large, or as robustly filled by HVC tracer injections as it is in males (compare Figure b,d). While we did not attempt volumetric reconstruction because female MMAN could only be clearly identified in 1 or 2 sagittal sections in individual birds, we note that male MMAN typically appears in 4 or 5 sagittal sections using the same section thickness and measurement of alternate sections (Elliott et al, ). Thus, it seems likely that zebra finch MMAN, along with HVC, RA, Area X, and NIf shows a M > F sex difference in size.…”

“…In adult males, HVC and RA are reciprocally connected—a small population of neurons in dorsal RA send and receive connectivity with HVC (Basista et al, ; Elliott et al, ; Roberts et al, ). In adult females, we did not observe retrogradely labeled cells in dorsal RA following HVC tracer injections.…”

“…To compare the morphology of regions providing afferent input to male and female HVC, tissue sections from N = 6 birds included in Elliott, Wu, Bertram, Hyson, and Johnson () were used. Briefly, these birds received visually guided tracer injections in HVC, using the heavy myelination that surrounds male HVC to precisely target the tracer injections.…”

“…These injections backfilled neurons in five different regions that provide afferent input to male HVC: RA, MMAN (medial magnocellular nucleus of the anterior nidopallium), Av, NIf (nucleus interfacialis), Uva (nucleus uvaeformis of the thalamus). See Elliott et al () for additional details.…”