Evolution of the basal ganglia: Dual‐output pathways conserved throughout vertebrate phylogeny

Abstract

The basal ganglia, including the striatum, globus pallidus interna and externa (GPe), subthalamic nucleus (STN), and substantia nigra pars compacta, are conserved throughout vertebrate phylogeny and have been suggested to form a common vertebrate mechanism for action selection. In mammals, this circuitry is further elaborated by the presence of a dual-output nucleus, the substantia nigra pars reticulata (SNr), and the presence of modulatory input from the cholinergic pedunculopontine nucleus (PPN). We sought to determine whether these additional components of the mammalian basal ganglia are also present in one of the phylogenetically oldest vertebrates, the lamprey. We show, by using immunohistochemistry, tract tracing, and whole-cell recordings, that homologs of the SNr and PPN are present in the lamprey. Thus the SNr receives direct projections from inwardly rectifying γ-aminobutyric acid (GABA)-ergic striatal neurons expressing substance P, but it is also influenced by indirect basal ganglia projections from the STN and potentially the GPe. Moreover, GABAergic SNr projection neurons are tonically active and project to the thalamus and brainstem motor areas. The homolog of the PPN contains both cholinergic and GABAergic neurons and is connected with all the nuclei of the basal ganglia, supporting its proposed role as part of an extended basal ganglia. A separate group of cholinergic neurons dorsal to the PPN corresponds to the descending mesencephalic locomotor region. Our results suggest that dual-output nuclei are part of the ancestral basal ganglia and that the PPN appears to have coevolved as part of a mechanism for action selection common to all vertebrates.

Independent circuits in the basal ganglia for the evaluation and selection of actions

“…A second fiber bundle left ventrally and progressed through the hypothalamus and appeared to terminate in the pedunculopontine nucleus (PPN) in the mesencephalon ( Fig. 3H), confirming previous studies showing that a few GPh neurons project to the PPN (20). No fibers were observed innervating the brainstem motor regions, including the optic tectum, torus semicircularis and mesencephalic locomotor region ( Fig.…”

“…The major projections of the GPh neurons are, therefore, to the homolog of the lateral habenula. These results indicate that, as with the input, the output circuitry of the GPh is completely distinct from the GPi/GPe, which projects to the thalamus and brainstem motor regions (11,(18)(19)(20). tegmental area (VTA) and the matriosomes that preferentially express calbindin along with a range of other neurotransmitterrelated substances (21)(22)(23).…”

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

“…8D) as in other species (54)(55)(56). Furthermore, the basal ganglia output nuclei instead provide tonic GABAergic inhibition to the tectal output cells in lamprey as well as in mammals (31,(57)(58)(59). This GABAergic input to the tectal output cells can serve to gate the circuit and allow activation through a temporary release from inhibition (disinhibition) (60).…”

“…There is also in lamprey a dopaminergic projection from the substantia nigra pars compacta, which will potentiate (via dopamine D 1 receptor) or suppress (via dopamine D 2 receptor) the responses of the tectal output neurons (62,63). Finally, there is cholinergic input from the parabigeminal nucleus (isthmic nucleus in nonmammals) that can modulate the visuomotor pathway through projections to the superficial layer (59,64).…”

Evolution of the forebrain — revisiting the pallium

“…But as was the case for birds, studies on molecular and hodological features of the forebrain in these fishes have led to the realization that pallial-equivalent cell groups are present despite the location of these groups below the ventricle (Wullimann and Mueller, 2004;Yamamoto et al, 2007;Northcutt, 2006;Nieuwenhuys, 2009;Mueller et al, 2011HarveyGirard et al, 2012Ganz et al, 2012). Recent hodological, neurochemical, and molecular studies suggest that lampreys also possess pallial and subpallial homologues (Murakami et al, 2001;Stephenson-Jones et al, 2012;Sugahara et al, 2013). Although several hypotheses have been proposed on the homology of lamprey pallial zones (Pombal et al, 2011), an unequivocal conclusion has yet to be reached.…”