COMMENTARYThe connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum
Introduction
The basal ganglia are a major neural system which receives inputs from virtually all cortical areas, and in turn affects the frontal cortex via its thalamic projections. The dopaminergic (DA) innervation of the basal ganglia plays a central role in a wide variety of motor, cognitive and emotional functions ascribed to the basal ganglia. This functional diversity is also reflected in the complexity of pathological conditions associated with DA dysfunction, such as Parkinson's disease, Tourette's syndrome and schizophrenia (e.g., Refs. 4., 47., 48., 81., 86., 89., 166., 195., 213., 214., 226., 267.). The striatum is a major contributor of basal ganglia input to the DA system and the major recipient of DA input. The understanding of the organization of the connections between the two systems is essential for unraveling their role in normal and pathological states.
Descriptions of the connections between the striatum and the DA system have relied primarily on the regional subdivision of the striatum into caudate, putamen and nucleus accumbens (NAcc). During the last 15 years, much of the work on these connections has been influenced by the compartmental organization of the striatum, but the relationship between the two levels of organization has not been fully delineated. Yet a different principle of striatal organization, namely, functional subdivision imposed by corticostriatal projections, has dominated the descriptions of striatal connections with the frontal cortex (via the pallidum, nigra and thalamus), which provide the basis for models of basal ganglia–thalamocortical organization. The functional subdivision of the striatum, however, has received scant attention with regard to the connections of the striatum with the DA system (but see Refs. 107., 163., 164., 165.). In parallel, different subdivisions are used for describing the DA system. For example, while anatomists usually subdivide this system according to cytoarchitectonic criteria, behavioral neuroscientists tend to use a subdivision based on efferent projections of the DA system (e.g., mesostriatal and mesolimbic DA systems). As a result, there is presently an abundance of nomenclatures used in the description of the striatal connections with the DA system. Moreover, different nomenclatures are preferentially used by researchers from different fields. This complexity is compounded by the fact that the same terms are often used in rodent and primate research, although it is not always clear that these terms represent analogous areas/subdivisions.
In the present work, we survey and compare the connections of the DA system with the striatum in rats and primates. We review data on the organization of these connections with respect to a tripartite functional (motor, associative and limbic) subdivision of the striatum, as well as with respect to its compartmental (patch/striosome–matrix) subdivision, and combine the two levels of organization. In addition, we briefly review the topography of the projections of the other basal ganglia nuclei to the DA system, with respect to their tripartite functional subdivision. We then combine the anatomical organization of basal ganglia projections to the DA system with data on DA cell physiology in order to advance an hypothesis on the influences of the basal ganglia on DA cell activity. Finally, we incorporate the striatal connections with the DA system into an open-interconnected scheme131., 132. of basal ganglia–thalamocortical circuitry.
Section snippets
The striatum
The striatum is the main input structure of the basal ganglia. It is divided into the dorsal striatum (neostriatum), which includes most of the caudate and putamen, and the ventral striatum, which comprises the NAcc, the ventromedial parts of the caudate and putamen, and the striatal part of the olfactory tubercle. An important characteristic of the dorsal striatum is its patch (striosome in primates)/matrix compartmental organization. These compartments can be distinguished on the basis of the
The mesencephalic dopaminergic system
The mesencephalic DA system is the largest DA system. The organization of DA neurons in rats and primates is generally similar, but there are some differences in the distribution of DA cells and in the extent of correspondence between DA cell groups and specific neuroanatomical regions.15., 58., 63., 78., 113., 173., 179., 234., 242.. Although DA cells form a continuous group,15., 26., 75., 78., 104., 113., 179., 210., 234., 235., 242. several parcellations of these neurons, based on different
The relations between the dopaminergic system and the functional subregions of the striatum
This section examines the topographical relations of the DA system with the limbic, associative and motor subregions of the striatum in rats and primates. It should be noted that, while our definition of the limbic striatum coincides with the terms limbic or ventral striatum as they are used in the literature, this is not the case with regard to the motor and associative striatum. In primates, the conventional distinction is between the putamen and the caudate rather than between motor and
Projections to the dopaminergic system from other nuclei of the basal ganglia
In addition to the massive striatal projections, the DA system receives basal ganglia inputs from the pallidum, the subthalamic nucleus (STN) and the SNR.
Functional implications: basal ganglia influences on dopamine cell activity
The synaptic organization of the DA innervation of the striatum and the effects exerted by DA on striatal neurons have been extensively reviewed (e.g., Refs. 83., 102., 202.). We will focus here on the influence of the basal ganglia on DA cells, with an emphasis on the differential inputs to cell bodies and proximal dendrites of nigral DA neurons and to their ventrally extending dendrites. Since much more is known on the subcellular targets of basal ganglia projections to the SN and on
The dopaminergic system and the open-interconnected organization of basal ganglia circuitry
In the last 15 years, the basal ganglia have been viewed as “components of basal ganglia–thalamocortical circuits that are organized in a parallel manner and remain largely segregated from one another, both structurally and functionally” (Ref. 6, p. 119; also see Refs. 5., 7., 47., 95., 97., 213.). Each circuit receives input from several separate but functionally related cortical areas, traverses specific regions of the striatum, GPi, SNR and thalamus, and projects back upon one of the
Acknowledgements
We are indebted to Prof. H. Groenewegen for critical reading of the manuscript. We also thank our anonymous referees for their constructive comments.
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