Organization of the songbird basal ganglia, including area X

Abstract

Area X is a songbird basal ganglia nucleus that is required for vocal learning. Both Area X and its immediate surround, the medial striatum (MSt), contain cells displaying either striatal or pallidal characteristics. We used pathway-tracing techniques to compare directly the targets of Area X and MSt with those of the lateral striatum (LSt) and globus pallidus (GP). We found that the zebra finch LSt projects to the GP, substantia nigra pars reticulata (SNr) and pars compacta (SNc), but not the thalamus. The GP is reciprocally connected with the subthalamic nucleus (STN) and projects to the SNr and motor thalamus analog, the ventral intermediate area (VIA). In contrast to the LSt, Area X and surrounding MSt project to the ventral pallidum (VP) and dorsal thalamus via pallidal-like neurons. A dorsal strip of the MSt contains spiny neurons that project to the VP. The MSt, but not Area X, projects to the ventral tegmental area (VTA) and SNc, but neither MSt nor Area X projects to the SNr. Largely distinct populations of SNc and VTA dopaminergic neurons innervate Area X and surrounding the MSt. Finally, we provide evidence consistent with an indirect pathway from the cerebellum to the basal ganglia, including Area X. Area X projections thus differ from those of the GP and LSt, but are similar to those of the MSt. These data clarify the relationships among different portions of the oscine basal ganglia as well as among the basal ganglia of birds and mammals.

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

“…In mammals, a similar rule has been found to describe synaptic connections from cortex to the basal ganglia (37). Thus, a causal inverse may reside in the efferent synapses of a cortical area upstream of the basal ganglia homolog; or, based on anatomy, a causal inverse could be connected to a dopaminergic ventral tegmental area (38,39), thereby establishing a possible link of our findings with reinforcement learning theories (see below). Other candidate pathways for the causal inverse could lead to LMAN through HVC or through the thalamo-cortical projections from the dorsolateral nucleus of the thalamus (DLM).…”

Evo-devo, deep homology and FoxP2: implications for the evolution of speech and language

“…Recording from Area X in singing birds, Goldberg et al [176] recently identified two types of these neurons, differing in connectivity and firing pattern, in a very similar way as do the two different pallidal neuron types in primates. Importantly, Area X within the songbird striatum has slightly different connectivity patterns than the surrounding striatum [177]. These differences could reflect the small evolutionary modifications postulated for new traits, such as avian vocal learning.…”

Song-related dopamine receptor regulation in Area X of zebra finch male

“…Learning and production of learned song patterns in songbirds is controlled by an anatomically discrete system of interconnected brain nuclei (Nottebohm et al 1976). The nucleus residing in songbird basal ganglia, Area X, receives the densest dopaminergic innervations among all song nuclei from the midbrain ventral tegmental area (VTA) and substantia nigra, pars compacta (SNc) (Lewis et al 1981;Person et al 2008). It also shows the highest expressions of the D1A, D1B, and D2 dopamine receptor mRNAs and these levels are higher than those in the surrounding striatum .…”