Histochemical demonstration and mapping of 5-hydroxytryptamine- and catecholamine-containing neuron systems in the human fetal brain

Olson, Lar̀s; Boréus, L. O.; Seiger, Åke

doi:10.1007/bf00519968

Cited by 251 publications

(70 citation statements)

References 41 publications

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“…The significance of this early afferent modulatory input for the early endogenous (Kostović, 1986;Kostović & Judaš, 2007), oscillatory activity of the cortex was stressed in recent experimental studies (Hanganu & Luhmann, 2004;Luhmann et al 2009;Yang et al 2009). The other modulatory inputs arriving at the telencephalon at very early ages are from the monoaminergic nuclei in the brainstem (Nobin & Bjorklund, 1973;Olson et al 1973;Molliver & Kristt, 1975;Zecevic & Verney, 1995). These earliest afferent pathways, visualized by fluorescent techniques, do not form distinct bundles, and are formed by extremely fine fibers.…”

Section: Discussion On Development Of Fiber Pathways In the Cerebral mentioning

confidence: 99%

“…Therefore, these pathways cannot be demonstrated by a tractography or by the histological techniques presented in this review. The only possible trajectory where these early monoaminergic afferents can be eventually visualized is the medial forebrain bundle in the lateral hypothalamus (Nauta, 1971;Nobin & Bjorklund, 1973;Olson et al 1973). …”

Section: Discussion On Development Of Fiber Pathways In the Cerebral mentioning

confidence: 99%

“…2A, double curved arrows). Other monoaminergic early afferents were demonstrated with monoamine-fluorescence techniques (Nobin & Bjorklund, 1973;Olson et al 1973;Zecevic & Verney, 1995). Early afferents from the thalamus form a massive bundle, the so-called cerebral stalk (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Development of axonal pathways in the human fetal fronto‐limbic brain: histochemical characterization and diffusion tensor imaging

et al. 2010

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The development of cortical axonal pathways in the human brain begins during the transition between the embryonic and fetal period, happens in a series of sequential events, and leads to the establishment of major long trajectories by the neonatal period. We have correlated histochemical markers (acetylcholinesterase (AChE) histochemistry, antibody against synaptic protein SNAP-25 (SNAP-25-immunoreactivity) and neurofilament 200) with the diffusion tensor imaging (DTI) database in order to make a reconstruction of the origin, growth pattern and termination of the pathways in the period between 8 and 34 postconceptual weeks (PCW). Histological sections revealed that the initial outgrowth and formation of joined trajectories of subcortico-frontal pathways (external capsule, cerebral stalk-internal capsule) and limbic bundles (fornix, stria terminalis, amygdaloid radiation) occur by 10 PCW. As early as 11 PCW, major afferent fibers invade the corticostriatal junction. At 13-14 PCW, axonal pathways from the thalamus and basal forebrain approach the deep moiety of the cortical plate, causing the first lamination. The period between 15 and 18 PCW is dominated by elaboration of the periventricular crossroads, sagittal strata and spread of fibers in the subplate and marginal zone. Tracing of fibers in the subplate with DTI is unsuccessful due to the isotropy of this zone. Penetration of the cortical plate occurs after 24-26 PCW. In conclusion, frontal axonal pathways form the periventricular crossroads, sagittal strata and 'waiting' compartments during the path-finding and penetration of the cortical plate. Histochemistry is advantageous in the demonstration of a growth pattern, whereas DTI is unique for demonstrating axonal trajectories. The complexity of fibers is the biological substrate of selective vulnerability of the fetal white matter.

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Section: Discussion On Development Of Fiber Pathways In the Cerebral mentioning

confidence: 99%

Section: Discussion On Development Of Fiber Pathways In the Cerebral mentioning

confidence: 99%

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Development of axonal pathways in the human fetal fronto‐limbic brain: histochemical characterization and diffusion tensor imaging

et al. 2010

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“…Soon after dopamine-containing fibers can be detected within the striatum, they cluster together in macroscopically visible groupings called "dopamine islands" (1)(2)(3)(4)(5). The predominant islandic organization of the nigrostriatal innervation continues into the early postnatal period.…”

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Differences in tyrosine hydroxylase-like immunoreactivity characterize the mesostriatal innervation of striosomes and extrastriosomal matrix at maturity.

Graybiel¹,

Hirsch²,

Agid³

1987

Proc. Natl. Acad. Sci. U.S.A.

100

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Tyrosine hydroxylase [TyrOHase, tyrosine 3-monooxygenase, L-tyrosine, tetrahydropteridine:oxygen oxidoreductase (2-hydroxylating), EC 1.14.16.2] is the ratelimiting enzyme in the synthetic pathway of catecholamines and is expressed by neurons containing dopamine, norepinephrine, and epinephrine. TyrOHase is present in high concentrations in the caudate nucleus and putamen, where nearly all of it is contained in axons of the dopaminergic mesostriatal pathways. We have employed three different polyclonal antibodies directed against TyrOHase, one tested here for specificity by twodimensional gel electrophoresis, to reexamine the anatomic distribution of fibers expressing TyrOHase-like immunoreactivity in the striatum of mature human, monkey, and cat brains. The findings suggest that this distribution is distinctly inhomogeneous. The macroscopic compartments known as striosomes have low TyrOHase-like immunoreactivity relative to the surrounding extrastriosomal matrix. These observations add to evidence that dopaminergic modulation of neural processing in the mature striatum is organized in accordance with striosomal architecture and suggest that part of the mechanism for such differentiation may involve presynaptic differences in enzymatic regulation of dopamine content in and out of striosomes.An apparently universal characteristic of the nigrostriatal system in mammals is that it undergoes a modular course of development. Soon after dopamine-containing fibers can be detected within the striatum, they cluster together in macroscopically visible groupings called "dopamine islands" (1-5). The predominant islandic organization of the nigrostriatal innervation continues into the early postnatal period. Gradually, however, there is an increase in the nonislandic dopamine-containing innervation until finally the early formed dopamine islands are no longer readily detectable (1, 6, 7).On the basis ofthese observations, Fuxe and his colleagues (1, 8) divided the nigrostriatal system into "diffuse" and "islandic" components. They further suggested that the islandic innervation persists into adulthood but is masked by the diffuse system, because when they treated adult rats with inhibitors of tyrosine hydroxylase [TyrOHase, tyrosine 3-monooxygenase, L-tyrosine, tetrahydropteridine:oxygen oxidoreductase (2-hydroxylating), EC 1.14.16.2] they could elicit reappearance of intensely fluorescent dopamine islands. They hypothesized that the islandic and diffuse systems have different rates of dopamine turnover, with that of the islandic system being lower.There is now direct experimental evidence that the islandic fiber system selectively innervates the striatal compartments known as striosomes (6, 9-11) and that the neurons giving rise to the islandic and the nonislandic innervations lie in different parts of the A8-A9-A10 cell complex of the midbrain (refs. 9-11; J. Jimenez-Castellanos and A.M.G., unpublished results). Further observations suggest that D1 dopamine receptor subtypes may be preferentially related to the isl...

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“…At least some of the dopamine-containing fibers do appear to be organized into compartments. In the fetal and neonatal striatum catecholamine fluorescence is localized in discrete patches or "islands" (11)(12)(13)(14) and, though fluorescence is broadly, and apparently evenly, dispersed in the striatum of the normal adult (11,12,(15)(16)(17), fluorescent islands have been observed by Fuxe and his colleagues (12,18) in the striatum ofrats pretreated with an inhibitor oftyrosine hydroxylase [tyrosine 3-monooxygenase; L-tyrosine,tetrahydropteridine:oxygen oxidoreductase (3-hydroxylating), EC 1.14.16.2]. In neither the young animals nor the adults, however, has a direct correlation been established between the dopamine islands and any other set of striatal patches.…”

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confidence: 99%

Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum.

Graybiel¹,

Pickel²,

Joh³

et al. 1981

Proc. Natl. Acad. Sci. U.S.A.

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The distribution of dopamine-containing processes in the striatum of fetal and neonatal cats was studied by immunohistochemical and glyoxylic acid histofluorescence methods and compared to the distribution of acetylcholinesterase (acetylcholine acetylhydrolase, EC 3.1.1.7) observed by thiocholine histochemistry in the same or serially adjoining sections. Both methods for demonstrating the dopamine innervation revealed the characteristic patchwork of dopamine "islands" in the caudoputamen, in which catecholamine histofluorescence or tyrosine hydroxylase [tyrosine 3-monooxygenase; L-tyrosine, tetrahydropteridine: oxygen oxidoreductase (3-hydroxylating), EC 1.14.16.21-like immunoreactivity was concentrated into 0.2-to 0.6-mm-wide patches. Both methods also demonstrated a high degree ofpatterning of the dopamine innervation in the ventral striatum, including the nucleus accumbens septi. A detailed and striking match was found between these configurations and the compartmental distribution of acetylcholinesterase observed in the caudoputamen and ventral striatum of the same brains. The correspondence between the dopamine and acetylcholinesterase figures was most obvious in the fetal brains, in which the background acetylcholinesterase staining was lightest, but matches between the dopamine islands and acetylcholinesterase patches could still be seen in the kittens. There was no clear alignment of striatal cell bodies stained for acetylcholinesterase with either the dopamine or the acetylcholinesterase-positive patches. Nor was there an obvious correspondence between dopamine and acetylcholinesterase in the striatal background matrix. We conclude that, at least during ontogenesis, it is the clustered arrangements of dopamine and acetylcholinesterase that are, in particular, tightly linked, and we suggest that information about the maturation of these clusters may be crucial in assessing the functions of striatal dopamine and acetylcholinesterase in the adult.A surprising outcome ofrecent work on the caudate nucleus and putamen is that these telencephalic nuclei, although subcortical, are divided up into orderly sets ofanatomical compartments with distinct histochemical properties and fiber connections. In the mature striatum, incoming afferents from the neocortex (1, 2) and thalamus (3-5), striatal projection cells (6), and certain neuropeptides (7) form three-dimensional patchworks, and we have shown that these heterogeneous distributions are for the most part aligned with a network of acetylcholinesterase (acetylcholine acetylhydrolase, EC 3.1.1.7)-poor zones called striosomes (8-10). The implications of these correspondences are ofat least two sorts. First, though electrophysiological evidence is still lacking, it is clear from the anatomy that these striosomal units must be functional units because they represent subdivisions in which connections become established between particular sets of striatal inputs and outputs. Second, the findings suggest that there is a compartmentalization of different pharmac...

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Histochemical demonstration and mapping of 5-hydroxytryptamine- and catecholamine-containing neuron systems in the human fetal brain

Cited by 251 publications

References 41 publications

Development of axonal pathways in the human fetal fronto‐limbic brain: histochemical characterization and diffusion tensor imaging

Development of axonal pathways in the human fetal fronto‐limbic brain: histochemical characterization and diffusion tensor imaging

Differences in tyrosine hydroxylase-like immunoreactivity characterize the mesostriatal innervation of striosomes and extrastriosomal matrix at maturity.

Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum.

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