Parallel executive pallio-motor loops in the pigeon brain

Abstract

A core component of the avian pallial cognitive network is the multimodal nidopallium caudolaterale (NCL) that is considered to be analogous to the mammalian prefrontal cortex (PFC). The NCL plays a key role in a multitude of executive tasks such as working memory, decision-making during navigation, and extinction learning in complex learning environments. Like the PFC, the NCL is positioned at the transition from ascending sensory to descending motor systems. For the latter, it sends descending premotor projections to the intermediate arcopallium (AI) and the medial striatum (MSt). To gain detailed insight into the organization of these projections, we conducted several retrograde and anterograde tracing experiments. First, we tested whether NCL neurons projecting to AI (NCL_arco neurons) and MSt (NCL_MSt neurons) are constituted by a single neuronal population with bifurcating neurons, or whether they form two distinct populations. Here, we found two distinct projection patterns to both target areas that were associated with different morphologies. Second, we revealed a weak topographic projection toward the medial and lateral striatum and a strong topographic projection toward AI with clearly distinguishable sensory termination fields. Third, we investigated the relationship between the descending NCL pathways to the arcopallium with those from the hyperpallium apicale, which harbors a second major descending pathway of the avian pallium. We embed our findings within a system of parallel pallio-motor loops that carry information from separate sensory modalities to different subpallial systems. Our results also provide insights into the evolution of the avian motor system from which, possibly, the song system has emerged.