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Anatomical Relationship Between the Basal Ganglia and the Basal Proc. Nati. Acad. Sci. USA Vol. 84, pp. 1408-1412, March 1987 Medical Sciences Anatomical relationship between the basal ganglia and the basal nucleus of Meynert in human and monkey forebrain (enkephalin/acetylcholinesterase/primate/human) SUZANNE HABER Department of Neurobiology and Anatomy, University of Rochester, Rochester, NY 14642 Communicated by Walle J. H. Nauta, October 20, 1986 ABSTRACT Previous immunohistochemical studies have suggestion that the basal ganglia could serve cognitive as well provided evidence that the external segment of the globus as motor functions (7). Because this notion places the basal pallidus extends ventrally beneath the transverse limb of the ganglia in a functional category comparable, in part at least, anterior commissure into the area of the substantia in- to that of the basal nucleus of Meynert, a more detailed nominata. Enkephalin-positive staining in the form of "woolly description ofthe relationship ofthese two structures to each fibers" has been used as a marker for the globus pallidus and other seemed of interest. its ventral extension. Acetylcholinesterase staining of both The globus pallidus (in particular its most ventral part, the fibers and cell bodies, frequently used as a marker for the basal ventral pallidum) and the basal nucleus of Meynert are nucleus of Meynert, is also found in the area of the substantia adjacent structures (Fig. 2 A-C and 3 A and B). The large innominata. This study describes the differential distribution of acetylcholinesterase (AcChoEase)-positive neurons in the enkephalin-positive woolly fibers and acetylcholinesterase substantia innominata (i.e., the infrapallidal region of the staining on adjacent sections in both the monkey and human basal forebrain) are regarded as a characteristic marker for basal forebrain area in an attempt to define the relationship the basal nucleus of Meynert and are therefore considered to between the basal ganglia and the basal nucleus of Meynert. define the nucleus in the monkey and human brain (8, 9). On The results show that while both occupy large regions of the the other hand, enkephalin-staining in the form of "woolly basal forebrain, they overlap very little. In both species fibers" [enkephalin-positive striatal efferents ensheathing investigated, dense concentrations of acetylcholinesterase-pos- each of the long dendrites of pallidal neurons individually itive neurons lie, for the most part, outside the boundaries of (Fig. 1)] has become recognized as an equally characteristic the pallidal fibers. However, some scattered acetylcholines- marker for the globus pallidus in the rat, monkey, and human terase cells do lie within the confines ofthe dorsal pallidum, and forebrain (10-12). Large AcChoEase-positive neurons have a more prominent group is found in the subcommissural been found within the boundaries of the globus pallidus in a ventral pallidum. These cells may constitute a group separate distribution continuous with that of the basal nucleus of from the more densely packed acetylcholinesterase-positive Meynert. Such cells are particularly numerous in a ventral cells in woolly fiber-free regions in that they may receive direct region of the globus pallidus and the ventral pallidum of striatal input. Heimer and Wilson (13) but also occur, more sparsely distributed, in more dorsal pallidal regions. It was initially Parkinson disease and senile dementia of the Alzheimer type assumed that these intrapallidal elements ofthe basal nucleus are two degenerative disorders that occur in mid to late life. ofMeynert are foreign to the globus pallidus and unrelated to Whereas each disease is associated with a specific symptom- the circuitry of the basal ganglia. Recent findings in the rat atology and pathology, a number of cases have recently been forebrain, however, suggest that at least some of these described in which some overlap ofboth disorders is evident intrapallidal cholinergic neurons receive afferents from the (1-3). For example, a patient may initially exhibit classical striatum (14-16). Such a connection would provide a direct Parkinson-like motor disabilities and later exhibit dementia linkage of the basal ganglia to the basal nucleus of Meynert. characteristic ofAlzheimer disease. Furthermore, cases have This study demonstrates the extent to which the striatal been described in which patients with the symptoms of one projection to the globus pallidus (as defined by enkephalin- disease were found to have the pathology that characterizes positive woolly fibers), and the basal nucleus of Meynert (as the other disease, either in addition to, or in the absence of, defined by its AcChoEase-positive neurons), overlap in the the pathology of the diagnosed disease. human and nonhuman primate brain. The rationale for the has been known to reflect a disor- study was the assumption that striatal efferents establish Parkinson disease long synaptic contact with neurons in the basal nucleus of der of the basal ganglia, whereas Alzheimer disease has Meynert only within such areas of overlap. Moreover, it recently become widely attributed, at least in part, to a seemed possible that pathology affecting the function of such pathology of the basal nucleus of Meynert (4). The basal areas might be reflected in symptoms that represent both ganglia (composed primarily of the striatum and globus Parkinson and Alzheimer disease. pallidus) and the basal nucleus of Meynert are traditionally viewed as separate functional entities-the former involved in somatic movement, the latter associated with cognitive EXPERIMENTAL PROCEDURES functions. Recent anatorhical findings, however, have raised Five brains from neurologically normal patients were ob- questions regarding a purely motoric function of the basal tained between 8 and 10 hr after death. Coronal slabs of ganglia; in particular, the existence ofconnections linking the approximately 15-mm thickness were cut immediately, fixed striatopallidal complex not only to the motor cortex but also by immersion in buffered fornialin for 2 weeks, then trans- to the prefrontal cortex (5-7) and amygdala has led to the ferred from lower to higher concentrations of sucrose (5%, 10%, and 20%), and finally stored in 30% sucrose in 0.1 M The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviations: AcChoEase, acetylcholinesterase; ChoAcTase, in accordance with 18 U.S.C. §1734 solely to indicate this fact. choline acetyltransferase. Downloaded by guest on September 29, 2021 1408 Medical Sciences: Haber Proc. Natl. Acad. Sci. USA 84 (1987) 1409 a drawing tube. The drawing was then photographically reduced and taped to the wall for projection of the adjacent ill enkephalin-stained section onto it. To further verify regions of overlap the two sections were viewed on separate micro- I. scopes equipped with a Leitz comparator bridge to allow superimposition of the images from the two slides. Finally, key sections were double-stained by the fluorescent-antibody method and the Geneser-Jensen and Blackstad technique for AcChoEase to verify the observations in the adjacent sec- tions. Due to the weak and fading fluorescence it was difficult A' to analyze double-stained sections in detail. 0. RESULTS I Numerous large AcChoEase-positive neurons were found in 1. t ~ the basal forebrain of all brains examined. Their distribution a;*I r pattern was consistent with that described previously (8, 9). In areas 4 many the individual cell bodies were somewhat ., 0 obscured by the vast number of cholinergic fibers passing through the region; within such areas the actual number of AcChoEase-positive neurons may have been underestimat- ed. Adjacent Nissl-stained sections confirmed the location and distribution of these neurons originally described by Meynert in 1872 (20). Enkephalin-like immunoreactivity appeared in its characteristic pattern of woolly fibers in the region of the globus pallidus. Fig. 2 A-C illustrates the relationship between the enkeph- alin-positive fibers and the AcChoEase-positive neurons in FIG. 1. Single enkephalin-positive striatal efferent fiber joining the monkey forebrain, and Fig. 3 A-E illustrates this in the other fibers wrapping a pallidal dendrite to form a woolly fiber. Open human forebrain. arrow indicates single efferent fiber; filled arrow indicates woolly In the human brain, large AcChoEase-positive neurons fiber. appear within the fiber laminae forming the boundaries ofthe globus pallidus. Such cells are found within the internal phosphate buffer, pH 7.2 for 1-3 days. Four adult African capsule and within both the external medullary lamina that green monkeys (Cercopithecus aethiops) were anesthetized separates the putamen from the external segment of the and perfused with 4% paraformaldehyde, and their brains globus pallidus and the internal medullary lamina that sepa- were then transferred through the concentrations of sucrose rates the external and internal pallidal segments. Whereas listed above. these cells are distributed throughout the thickness of the Antisera to enkephalin were provided by R. Elde (Univer- laminae, most are located directly adjacent to the external sity of Minnesota). Characterization of these antibodies has segment of the globus pallidus (Figs. 2A and 3B). A few been described in detail elsewhere (17). These antisera do not scattered AcChoEase-positive magnocellular neurons are cross-react with either ofthe other two classes ofendogenous also seen within the
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