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Keywords:

  • subplate zone;
  • thalamocortical system;
  • acetylcholinesterase;
  • associative connections

Abstract

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

Transient patterns of regional, laminar, modular, neuronal, and functional organization are essential features of the developing cerebral cortex in preterm infants. Analysis of cytological, histological, histochemical, functional, and behavioral parameters revealed that transient cerebral patterns develop and change rapidly between 24 weeks post ovulation (W) and birth. The major afferent fibers (thalamocortical, basal forebrain, and corticocortical) grow through the transient “waiting” subplate zone (SP) compartment and accumulate below the cortical plate (CP) between 22 and 26 W. These afferent fibers gradually penetrate the CP after 26 W. The prolonged process of dissolution of the SP can be explained by prolonged growth and maturation of associative connections in the human cerebral cortex. The neurons and circuitry elements of the transient layers are the substrate for transient functional and behavioral patterns. The predominance of deep synapses and deep dendritic maturation underlies the immaturity and different polarity of the cortical electrical response in the preterm infant. The significant changes in the transient SP, together with profound changes in the transient architecture of the neocortical plate, parallel the changes observed in recent MRI studies. The role of the SP in the formation of cortical connections and functions is an important factor in considering the pathogenesis of cognitive deficits after brain lesions in the preterm infant. Anat Rec 267:1–6, 2002. © 2002 Wiley-Liss, Inc.

The prenatal development of the cerebral cortex is characterized by transient patterns of regional, laminar, modular, and neuronal organization (Kostović, 1990a). Whereas the transient patterns of the laminar organization and neuronal circuitry elements have been well documented in both classical (His, 1904; Boulder Committee, 1970) and more recent (Marin-Padilla, 1988; Kostović, 1990a; Rakic, 1995) literature, the majority of recent studies have focused on the transient patterns of the regional and areal organization involved in the processes of early areal specification and genetic control of cortical development (Rubenstein and Rakic, 1999). For example, it was recently shown that the early specification of some human cortical areas and regions occurs even before 18 weeks post ovulation (W), i.e., before the establishment of thalamocortical connections (Kostović et al., 1993; Šestan et al., 1998). The available evidence clearly shows that the organization of the prenatal cerebral cortex differs substantially from that in the postnatal period with respect to both its cellular constituents and their areal, laminar, and modular arrangement, and their role in changing patterns of neuronal circuits (Kostović, 1990a, b; Kostović and Rakic, 1990; Rakic, 1995; Ulfig et al., 2000). Indeed, a variety of histogenetically important structures in the human fetal brain have a transient nature as well as a specific spatio-temporal pattern of development, suggesting that these structures have specific developmental roles in the establishment of the adult-like pattern of the structural and functional organization of the human cerebral cortex (Kostović, 1990b; Ulfig et al., 2000). Furthermore, the transient patterns of organization represent one of the key differences between the cortex of prematurely born, low-birth-weight infants, and infants born at term (Kostović, 1990a, b; Volpe, 1996, 2000). Although some of these differences have been described in recent in vivo magnetic resonance imaging (MRI) studies of preterm and term infant brains (Hüppi et al., 1998; Inder and Hüppi, 2000), our knowledge of the complex transformations of the patterns of cortical organization during the late prenatal and perinatal periods is still fragmentary and incomplete. In fact, the potential advantages of in vivo MRI studies, which have recently opened a window into the developing human brain (Inder and Hüppi, 2000), probably cannot be fully exploited without correlation with detailed histological studies of post-mortem specimens (Kostović et al., 2000).

A detailed cytological, histological, and histochemical analysis of the developing human brain is necessary for a proper interpretation of the neurobiological basis of the rapid changes and transient patterns of cortical electrophysiology and behavioral states in prematurely born infants (Weitzman and Graziani, 1968; Nolte and Haas, 1978; Dreyfus-Brisac, 1979; Kurtzberg et al., 1984; Novak et al., 1989). A thorough knowledge of the developmental history of the transient subplate zone (SP) (Kostović and Rakic, 1990) is particularly important because the SP serves as a “waiting” compartment for various systems of ingrowing cortical afferent fibers, and the large population of early-generated SP neurons represents a prominent source of synaptic and other cellular interactions during the establishment of the functional, but transient, neuronal circuitry of the fetal cerebral cortex (Kostović and Rakic, 1990; Allendoerfer and Shatz, 1994; O'Leary et al., 1994; Ulfig et al., 2000).

The main purpose of this review is to describe and interpret changes in the SP in relation to the development of axon strata situated in the intermediate zone (IZ) below the SP, as well as in relation to the neuronal and synaptic differentiation of the cortical plate (CP) situated above the SP. The histological descriptions of the human cerebrum are derived from post-mortem material of fetuses and preterm infants (the material was collected after spontaneous abortions due to non-neurological causes). These specimens are part of our extensive Zagreb Neuroembryological Collection (Kostović et al., 1991), which encompasses more than 300 “normal” specimens of various prenatal ages, as well as more than 200 prenatal specimens with clinically and neuropathologically verified ischemic-hypoxic lesions and genetic malformations of the cerebral cortex. Thus, as best as could be assessed, our observations of preterm post-mortem material can be generalized to the normal prenatal brain at equivalent ages.

CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

Acetylcholinesterase (AChE) histochemistry is one of the few, but very effective, methods available for studying the development of thalamocortical and basal forebrain afferents in the human cerebral cortex. The successful application of this method has already enabled us to offer detailed descriptions of developing projections from the thalamus to the frontal, visual, and auditory cortex (Kostović and Goldman-Rakic, 1983; Krmpotić-Nemanić et al., 1983; Kostović and Rakic, 1984, 1990). In this work we review our data on the prenatal development of AChE-reactive afferent fibers of premotor and sensory-motor cortical regions.

Before 22 W, AChE-reactive afferent axons involved in the formation of the fibrillar plexus within the SP originate mainly from the internal capsule system and approach the SP through the IZ, i.e., the fetal “white” matter (Fig. 1A). In addition, AChE-reactive fibers originating from the basal forebrain approach the SP as a component of the external capsule system (Fig. 1A). In very premature newborn infants (22–26 W), these AChE-reactive fibers accumulate in the upper (superficial) SP and gradually begin to penetrate into the overlying CP. However, a massive contingent of AChE-negative fibers from the callosal radiation obviously contributes to the fibrillar plexus of the SP (Fig. 1A–C), causing a decrease in intensity of the AChE staining in the deep part of the SP. The relative importance of callosal afferents in the overall shaping of the SP can be best visualized in the occipital lobe, where the SP is very thick in the developing dorsolateral associative visual cortex with rich callosal input. The SP is much narrower in the developing medial primary visual cortex, which does not receive a significant callosal input (Kostović and Rakic, 1984, 1990).

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Figure 1. AChE-stained coronal sections through the telencephalon of human fetuses aged 18–32 W, with superimposed drawings displaying a transient arrangement of major cortical afferent fiber systems in the fetal IZ and SP: basal forebrain afferents (solid lines), thalamocortical afferents (dashed lines), callosal afferents (dotted lines), and ipsilateral long association fibers (dotted and dashed lines). A: In an 18-week-old fetus, all afferents grow through the IZ and penetrate the “waiting” compartment of the SP. B: In a 24-week-old fetus, basal forebrain afferents and a massive contingent of thalamocortical afferents have accumulated in the upper SP, just below the CP. C: In a 28-week-old fetus, the development of the SP reaches its peak. The transient arrangement of cortical afferent systems can be described as follows: thalamocortical and basal forebrain fibers have already largely penetrated the CP (thus contributing to its AChE staining), while callosal and ipsilateral associative fibers still predominantly reside in the transient “waiting” compartment of the SP. The dotted circle marks the approximate location of the long associative superior fronto-occipital bundle. D: In a 32-week-old fetus, there is an intense branching of thalamocortical fiber terminals within the CP, as well as the concomitant relocation of callosal and associative fibers from the SP into the CP. Therefore, the SP gradually diminishes in size, and its dissolution is especially prominent at the bottom of the cortical sulci.

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In the sensory-motor cortical region, the growth pattern of the thalamocortical afferents through the SP, including their accumulation in the superficial SP (Fig. 1B) and gradual penetration into the CP, is similar to the pattern of the thalamocortical system development already described in the prefrontal, visual, and auditory cortical areas (Kostović and Goldman-Rakic, 1983; Krmpotić-Nemanić et al., 1983; Kostović and Rakic, 1984). However, the AChE staining intensity is less pronounced in the sensory-motor region, probably because the ventroposterolateral thalamic nucleus displays moderate AChE reactivity in comparison with the thalamic nuclei projecting to the prefrontal, visual, and auditory cortical region. In addition, the contribution of afferent fibers from the highly AChE-reactive mediodorsal thalamic nucleus seems to be very limited in the motor and premotor cortices in comparison with the densely innervated prefrontal cortex.

During the same developmental ages (18–26 W), the SP and its cells can be successfully visualized with some other histochemical methods, such as NADPH-diaphorase histochemistry (Judaš et al., 1999) and PAS-Alcian Blue histochemistry (Kostović et al., unpublished communication). These methods enable a clear delineation of the SP, on the basis of the characteristic diffuse background staining of the SP neuropil (NADPH-d histochemistry), or because of selective staining of the acid-sulfated glycoconjugates of the SP extracellular matrix (PAS-Alcian Blue histochemistry). In addition, NADPH-d histochemistry enables the Golgi-like visualization of a large subpopulation of nitrinergic subplate neurons. These methods do not permit a selective visualization of thalamocortical or corticocortical fibers. However, the use of other immunocytochemical markers during the limited developmental period has confirmed the findings obtained with AChE histochemistry (Letinić et al., 1998).

The SP attains its maximum size at 28–30 W (Fig. 1C) (Kostović et al., 1989; Kostović 1990a; Kostović and Rakic, 1990; Kostović et al., 2000). During this period, the frontal cortex is characterized by the transient columnar arrangement of AChE reactivity within the CP (Kostović, 1990a) and dense AChE staining of the CP.

The relocation of thalamocortical fibers from the SP into the CP is accompanied by a corresponding shift in AChE reactivity (Fig. 1C). However, the SP retains its thickness and voluminous appearance, which may be explained by the continuous addition of AChE-negative callosal and other associative (ipsilateral) corticocortical afferents. It should be pointed out that at this developmental age the callosal fiber system is very prominent and occupies about one-third of the whole cerebral wall thickness. Among the ipsilateral corticocortical fiber systems, the long associative fronto-occipital fascicle is especially prominent, and is located lateral to the anterior horn of the lateral ventricle; this can even be visualized on T1-weighted MRI slices of brains from this developmental age (Kostović et al., 2000).

During the subsequent development, the SP in the sensory-motor cortex becomes very narrow at the bottom of the cortical sulci while retaining its thickness within the gyral crests (Fig. 1D). Moreover, the SP of the sensory-motor region is generally thinner in comparison with the SP of the frontal and parieto-occipital associative cortical regions. The process of SP dissolution accelerates after 34 W.

CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

After 24 W, the majority of cortical neurons have already settled within the CP and assumed laminar positions corresponding to the future layers II–VI. However, on the basis of both qualitative and quantitative criteria, deep cortical neurons are obviously more mature than superficial neurons (Mrzljak et al., 1988, 1990, 1992). This earlier maturation of the dendritic tree of deep cortical neurons occurs concomitantly with the penetration of thalamocortical fibers and the initial synaptogenesis within the deep part of the CP (Molliver et al., 1973, Kostović and Molliver, 1974; Kostović and Rakic, 1990). Since synapses are already present in the whole SP, and now appear in the deep part of the CP, there is an overall predominance of deep synapses in the neocortical anlage. In contrast, in later developmental stages a gradual shift in synaptogenesis and synaptic activity from predominantly deep to superficial cortical layers is observed. Therefore, the cortical electrical dipole changes, which may explain changes in the recorded cortical surface potentials observed in the corresponding stages of corticogenesis in the fetal dog (Molliver and Van der Loos, 1970), as well as in the characteristic and transient immature cortical response described in human premature infants (Dreyfus-Brissac, 1979; Novak et al., 1989). For example, a characteristic pattern of a very early stage of bioelectrical development (24–27 W) is the discontinuous bioelectrical activity with burst discharges (Dreyfus-Brisac, 1968). The EEG of a 27-week-old premature infant is mainly discontinuous; interburst intervals tend to decrease with increasing conceptional age, and the bursts are synchronous between hemispheres in 80–100% of recording epochs (Anderson et al., 1985). The main features of EEG maturation in preterm infants (29–38 W) are a progressive spatio-temporal differentiation, a decrease in discontinuous activity with burst discharges, and an increase in various rhythmic activities (Nolte and Haas, 1978; Cioni et al., 1992; reviewed in Kostović et al., 1995).

The developmental peak of the SP (28–30 W) sees the onset of intense dendritic differentiation of layer III cortical neurons, concomitant with the penetration of various classes of afferent fibers in the CP. This suggests that ingrowing afferents may be involved in the induction of the dendritic differentiation of cortical neurons between 27 and 32 W. The ingrowth of commissural and associative corticocortical fibers may also explain the rapid increase in length and arborization of the basal dendrites of layer III cortical neurons during this period, as these neurons are both the main source and the target of corticocortical connectivity (Mrzljak et al., 1990, 1992).

CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

In the adult neocortex, layer IV is the major recipient of thalamocortical afferents. Therefore, the developmental appearance or disappearance of layer IV granularity could serve as an important indicator of architectonic maturation of the CP. In preterm infants, the prospective granular layer IV is well developed in all neocortical areas, including the future agranular and dysgranular areas of the motor-premotor belt (Kostović, 1990a; Kostović et al., 1987). This was previously observed by Brodmann (1909), who described a six-layered ontogenetic Grundtypus in all neocortical areas of the cerebral cortex in preterm infants. Similar findings were also reported for equivalent ages in the developing sensorimotor cortex of the rhesus monkey (Huntley and Jones, 1991). However, after 34 W, the distinctness and granularity of layer IV gradually diminish in the premotor cortex, and layer IV disappears completely in the primary motor cortex (Kostović et al., 1987). Thus, the development of dysgranular and agranular cortical areas by diminution and/or disappearance of layer IV represents the most important cytoarchitectonic change in the developing cortex after 34 W. There is experimental evidence of the involvement of subplate neurons in the shaping of layer IV in the visual cortex of the cat, and of their role in the segregation of geniculocortical afferents during the critical period (Ghosh and Shatz, 1992, 1994). It is therefore reasonable to assume that subplate neurons are also involved in the perinatal shaping of layer IV in the human motor and premotor cortex.

CONCLUSIONS

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

The available evidence clearly shows that the period between 24 W and birth at term is characterized by profound changes in the patterns of the transient organization of both the SP and the CP, accompanied by distinct changes in the transient patterns of cortical bioelectrical activity and infant behavior (reviewed in Kostović et al., 1995). We suggest that the changes occurring in the SP are important because they reflect the pattern of development of the thalamocortical system (Kostović and Rakic, 1984, 1990). The developing fibers of this system transiently express specific chemical markers in specific developmental periods within the SP and the CP. The importance of thalamocortical afferents for molecular interactions between growing axons, transient subplate neurons, and target neurons in the CP, and for later phases of cortical areal specification, has been amply documented in various experimental studies in mammals (Allendoerfer and Shatz, 1994; Bicknese et al., 1994; O'Leary et al., 1994; Gao et al., 1998; Braisted et al., 2000).

In addition to thalamocortical afferents, the SP contains other major systems of cortical afferents, such as those originating from the basal forebrain (Kostović, 1986), monoaminergic brainstem nuclei (Verney, 1999), contralateral cerebral hemisphere (Schwartz and Goldman-Rakic, 1991), and ipsilateral corticocortical fibers. Thus, the SP appears to be highly involved in the differentiation of the cerebral cortex based on interactions with ingrowing axon systems. The role of the SP in the proper guidance and targeting of thalamocortical afferents to their final CP targets is well documented (Allendoerfer and Shatz, 1994; O'Leary et al., 1994; Braisted et al., 2000). It seems probable that other, non-thalamic cortical afferents need similar and complex molecular and cellular interactions to locate and recognize their proper cortical postsynaptic targets. The SP serves as a “waiting” compartment for all these classes of cortical afferents, thus providing ample opportunity for multiple interactions of these afferent fibers with surrounding cellular elements. However, the SP obviously has multiple developmental roles. For example, the neurons of the SP take part in the establishment of early and transient cortical neuronal circuits, and serve as pioneer neurons in the establishment of cortico-subcortical projections (Kostović and Rakic, 1990; Allendoerfer and Shatz, 1994; O'Leary et al., 1994; Ulfig et al., 2000). Therefore, the SP is probably of great functional significance during the corresponding stages of development of the premature infant brain (Volpe, 1996, 2000). For example, the majority of deep synapses in the midfetal human cortex are formed on neurons of the SP, and we have already emphasized the significance of predominantly deep synaptic elements and events between 22 and 28 W. Although the synaptogenesis in the human cortical anlage begins very early (around 8 W (Molliver et al., 1973; Kostović and Molliver, 1974)), it continues in essentially bilaminar fashion up to 28 W, with distribution of synaptic elements and their corresponding dendritic targets above and below the CP, and with a predominance of deep synapses. The bilaminar pattern of the synaptic distribution gradually disappears after 28 W, in parallel with the synaptogenesis in the superficial CP and the differentiation of layer III pyramidal neurons.

It is important to note that the deep source of electrical activity prevails throughout the period of very preterm infants, causing the immaturity of cortical electrical response (Kostović et al., 1995). This simple fact has remained largely unnoticed in numerous studies of electrophysiological development in preterm infants. However, the data presented in this and other works strongly suggest that deep synaptogenesis, together with the establishment of thalamocortical circuitry, is crucial for the transient patterns of organization of cortical connectivity in preterm infants. Whereas synaptogenesis predominantly occurs postnatally, the initial, prenatal synaptogenesis is vital for the establishment of functional circuitry elements and signaling pathways in the cerebral cortex.

When considering the pathogenesis of cognitive deficits after brain lesions in preterm infants, one should take into account the role of the SP and its neurons in the formation of cortical connections and the functioning of transient fetal circuits (Kostović et al., 1989; Volpe, 1996, 2000). It is interesting to note that abnormalities of subplate neurons have been recently implicated in the pathogenesis of schizophrenia (Bloom, 1993; Jones, 1997).

Finally, a 50% increase in the volume of the cortical gray matter between 29 W and term, with an acceleration of its growth after 28 W, has been recently documented in in vivo MRI studies of preterm infant brain development. This was interpreted as neuronal differentiation within the CP rather than an increase in the number of cortical neurons (Hüppi et al., 1998). Our data suggest that such an interpretation should be corrected and supplemented by taking into account the following facts: in the same period, a massive contingent of afferent fibers relocate from the SP into the CP and begin to branch extensively, thus contributing to the increase in the volume of the CP. Furthermore, the growth of callosal and long associative corticocortical fiber systems is protracted and continues intensely during the late prenatal period. In conclusion, the growth spurt of surface and volume in cortical gray matter observed from 28 W to term is based on ingrowth and arborization of thalamocortical and other cortical afferents, with concomitant elaboration of dendritic trees of main cortical pyramidal neurons (Mrzljak et al., 1988, 1990, 1992). These ongoing histogenetic processes significantly contribute to the increase in volume of the cortical neuropil.

Acknowledgements

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED

We acknowledge the skillful technical assistance of Zdenka Cmuk, Danica Budinšćak, and Danica Popović in the preparation of histological sections, and of Pero Hrabač in the preparation of the illustrations. This research was supported by the Croatian Ministry of Science and Technology, grant 0108118 (to principal investigator I.K.), and by a Zagreb Neuroembryological Collection grant 0108115 (to principal investigator M.J.).

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. CHANGES IN THE LAMINAR DISTRIBUTION OF MAJOR AFFERENT FIBERS
  4. CHANGES IN THE RATIO OF DEEP-TO-SUPERFICIAL PREDOMINANCE OF SYNAPSES AND DENDRITES
  5. CHANGES IN THE BASIC ARCHITECTURE OF THE NEOCORTICAL PLATE
  6. CONCLUSIONS
  7. Acknowledgements
  8. LITERATURE CITED
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