Evolution of the basal ganglia: new perspectives through a comparative approach

Abstract

The basal ganglia (BG) have received much attention during the last 3 decades mainly because of their clinical relevance. Our understanding of their structure, organisation and function in terms of chemoarchitecture, compartmentalisation, connections and receptor localisation has increased equally. Most of the research has been focused on the mammalian BG, but a considerable number of studies have been carried out in nonmammalian vertebrates, in particular reptiles and birds. The BG of the latter 2 classes of vertebrates, which together with mammals constitute the amniotic vertebrates, have been thoroughly studied by means of tract-tracing and immunohistochemical techniques. The terminology used for amniotic BG structures has frequently been adopted to indicate putative corresponding structures in the brain of anamniotes, i.e. amphibians and fishes, but data for such a comparison were, until recently, almost totally lacking. It has been proposed several times that the occurrence of well developed BG structures probably constitutes a landmark in the anamniote-amniote transition. However, our recent studies of connections, chemoarchitecture and development of the basal forebrain of amphibians have revealed that tetrapod vertebrates share a common pattern of BG organisation. This pattern includes the existence of dorsal and ventral striatopallidal systems, reciprocal connections between the striatopallidal complex and the diencephalic and mesencephalic basal plate (striatonigral and nigrostriatal projections), and descending pathways from the striatopallidal system to the midbrain tectum and reticular formation. The connectional similarities are paralleled by similarities in the distribution of chemical markers of striatal and pallidal structures such as dopamine, substance P and enkephalin, as well as by similarities in development and expression of homeobox genes. On the other hand, a major evolutionary trend is the progressive involvement of the cortex in the processing of the thalamic sensory information relayed to the BG of tetrapods. By using the comparative approach, new insights have been gained with respect to certain features of the BG of vertebrates in general, such as the segmental organisation of the midbrain dopaminergic cell groups, the occurrence of large numbers of dopaminergic cell bodies within the telencephalon itself and the variability in, among others, connectivity and chemoarchitecture. However, the intriguing question whether the basal forebrain organisation of nontetrapods differs essentially from that observed in tetrapods still needs to be answered.

A descending dopamine pathway conserved from basal vertebrates to mammals

“…In contrast, in rats, one remarkable aspect of our findings is that the vast majority of the DA neurons that project to the striatum also project to the MLR, implying a simultaneous ascending and descending modulation of the entire locomotor command circuitry from cortex to brainstem. These DA neurons are mostly located in the SNc with a few in the RRF, two structures that are classically considered as mesencephalic but that also span in the diencephalon (16,19,20). In lampreys, the terminology "mesodiencephalic DA neurons" does not apply, given that the DA neurons are all located in the diencephalon (40).…”

“…In lampreys and teleosts, those neurons are located only in the diencephalon (posterior tuberculum), but in tetrapods and cartilaginous fishes (14) they are located in both the diencephalon and the mesencephalon. An increasing number of authors seem to agree with the hypothesis that at least some of the mesodiencephalic DA neurons located in the diencephalon are homologous in all vertebrates, and thus, homologous to at least a portion of the mammalian substantia nigra pars compacta (SNc)/ ventral tegmental area (VTA) (13,(15)(16)(17)(18)(19); for review, see ref. 20).…”

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

“…The dorsal portion consists of the STR (caudate putamen in most mammals) and the dorsal pallidum, while the ventral portion consists of the NAcc and VP. It was previously thought that the basal ganglia were only present in amniotes (MacLean, 1990), but many studies in the past decade have shown that amphibians clearly possess the basal ganglia regions (Smeets et al, 2000) and teleosts likely do so as well (Wullimann and Mueller, 2004). In the following, we focus mainly on neurochemical, developmental, and hodological studies to support homologies across vertebrates, although we discuss lesion or stimulation studies where available in order to comment on whether these homologous structures are functionally similar.…”

“…Although both amphibians and teleosts lack a midbrain dopaminergic cell group (Smeets et al, 2000), multiple lines of evidence point to the posterior tuberculum, located in the ventral diencephalon, as the putative anamniote VTA homolog. Wullimann (2001, 2002) found that the posterior tuberculum is the teleost dopaminergic system ascending to the striatum, similar to mammals (Fallon and Moore, 1978), and suggested that this region in teleosts might be functionally similar and possibly homologous to the mammalian VTA/ substantia nigra pars compacta.…”

“…The basal ganglia constitute another area of contention, at least as far as anamniotes are concerned. These structures appear to be conserved at least across tetrapods (for review, see Smeets et al, 2000) and consist of a ventral and dorsal striatopallidal system (Heimer et al, 1995). The dorsal portion consists of the STR (caudate putamen in most mammals) and the dorsal pallidum, while the ventral portion consists of the NAcc and VP.…”