Organization of the avian “corticostriatal” projection system: A retrograde and anterograde pathway tracing study in pigeons

TLDR

Birds possess a well‑developed basal ganglia with a striatum comprising the lobus parolfactorius and paleostriatum augmentatum, yet the extent of cortical input to this system remains poorly understood; available evidence shows that pallial regions projecting to the striatum are part of higher‑order sensory or motor systems, and the corticostriatal network includes neurons that project to both striatum and brainstem as well as those that project only to striatum. Retrograde and anterograde tracing revealed that pigeons have a large continuous expanse of outer pallium—including the Wulst, archistriatum, and pallium externum—that projects to the striatum, with additional inputs from the caudolateral neostriatum, pyriform cortex, and hippocampal complex, while limbic pallial areas selectively target ventral striatal structures and specific striatal subregions, and the absence of such extensive projections in anamniotes points to an evolutionary emergence of the corticostriatal system in amniotes. © 1995 Wiley‑Liss, Inc.

Abstract

Abstract Birds have well‐developed basal ganglia within the telencephalon, including a striatum consisting of the medially located lobus parolfactorius (LPO) and the laterally located paleostriatum augmentatum (PA), Relatively little is known, however, about the extent and organization of the telencephalic “cortical” input to the avian basal ganglia (i. e., the avian “corticostriatal” projection system). Using retrograde and anterograde neuroanatomical pathway tracers to address this issue, we found that a large continuous expanse of the outer pallium projects to the striatum of the basal ganglia in pigeons. This expanse includes the Wulst and archistriatum as well as the entire outer rind of the pallium intervening between Wulst and archistriatum, termed by us the pallium externum (PE). In addition, the caudolateral neostriatum (NCL), pyriform cortex, and hippocampal complex also give rise to striatal projections in pigeon. A restricted number of these pallial regions (such as the “limbic” NCL, pyriform cortex, and ventral/caudal parts of the archistriatum) project to such ventral striatal structures as the olfactory tubercle (TO), nucleus accumbens (Ac), and bed nucleus of the stria terminalis (BNST). Such “limbic” pallial areas also project to medialmost LPO and lateralmost PA, while the hyperstriatum accessorium portion of the Wulst, the PE, and the dorsal parts of the archistriatum were found to project primarily to the remainder of LPO (the lateral two‐thirds) and PA (the medial four‐fifths). The available evidence indicates that the diverse pallial regions projecting to the striatum in birds, as in mammals, are parts of higher order sensory or motor systems. The extensive corticostriatal system in both birds and mammals appears to include two types of pallial neurons: (1) those that project to both striatum and brainstem (i. e., those in the Wulst and the archistriatum) and (2) those that project to striatum but not to brainstem (i. e., those in the PE). The lack of extensive corticostriatal projections from either type of neuron in anamniotes suggests that the anamniote‐amniote evolutionary transition was marked by the emergence of the corticostriatal projection system as a prominent source of sensory and motor information for the striatum, possibly facilitating the role of the basal ganglia in movement control. © 1995 Wiley‐Liss, Inc.