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Brain Behav Evol. 1995;46(4-5):235-58.

Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia.

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Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, Memphis 38163, USA.


The basal ganglia in modern mammals, birds and reptiles (i.e. modern amniotes) are very similar in connections and neurotransmitters, suggesting that the evolution of the basal ganglia in amniotes has been very conservative. For example, the basal ganglia in all amniotes possess a dorsal striatum containing two main populations of projection neurons, substance P-containing (SP+) and enkephalin-containing (ENK+) neurons, which have major projections to the dorsal pallidum and the tegmentum (ventral tegmental area and substantia nigra, or VTA/SN). The VTA/SN, in turn, has a major dopaminergic (DA+) projection to the striatum in all amniotes. In this paper, we review these data on the basal ganglia in amniotes and note points of similarity and difference in the functional circuitry of the basal ganglia among amniotes. In addition, we review recent findings on the neurotransmitter organization and connectivity of the basal ganglia in amphibians and fishes, with the goal of assessing whether a basal ganglia showing the same basic features as in amniotes is observed in anamniotes. Published data indicate that in at least two groups of fishes (cartilaginous fishes and lungfishes) and apparently in amphibians, the basal ganglia is present and consists of a distinct striatum and pallidum. The striatum of amphibians, cartilaginous fishes, and lungfishes contain SP+ and ENK+ neurons that seem to project to the pallidum as well as to a brainstem cell group that appears comparable to the VTA/SN of amniotes. Data for ray-finned fishes also suggest the presence of a striatum containing SP+ and ENK+ neurons that projects to VTA/SN-like brainstem cell group. In the basal ganglia of ray-finned fishes, however, a distinct pallidum had not been identified. Finally, the brainstem cell group receiving striatal input in all anamniotes contains DA+ neurons that seem to project to the striatum. The present analysis suggests that a rudimentary basal ganglia was already present in the brain of the ancestral jawed vertebrates. This rudimentary basal ganglia likely consisted of a striatum and a pallidum, and the striatum probably already possessed the same basic connections and some of the same basic cell types as the basal ganglia of modern jawed vertebrates.

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