OBJECTIVES (Revised) I. Introduction
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1 Neuroembryology: CNS Developmental Anomalies Raymond J. Colello, Ph.D. *Lecture written by Dr. John Povlishock Note: Emphasize Dr. Colello s lecture PPT and developmental anomalies OBJECTIVES (Revised) 1. Review basic neuroembryology 2. Review the differentiation of the neural tube into the CNS 3. Understand the differentiation of the alar plate into sensory structures (sensory cell columns), and basal plate into motor structures (motor cell columns), in the brainstem 4. Above the brainstem, trace the differentiation of the alar plate into forebrain structures, eg. thalamus, basal ganglia, cortex 5. Define causes of major developmental anomalies (eg. spina bifida, meningomyelocele, encephalocele, hydrocephalus, microgyria, agenesis of the corpus callosum, etc.) OBJECTIVES After studying the material presented in this lecture, the student should be capable of: 1. Discussing the basic developmental plan for the brain stem, appreciating the precise organization of the motor and sensory columns found within the basal and alar plates. 2. Describing in detail the development of the midbrain, pons, cerebellum and medulla. 3. Describing the basic developmental features of the forebrain. 4. Describing the general development of the telencephalon, appreciating the origin of five anatomical lobes of the brain as well as the basal ganglia. 5. Discussing the origin of the internal capsule and the major commissural systems. I. Introduction In humans, the nervous system and the neuro-epithelium of special sense organs are derived from embryonic ectoderm. The CNS (brain and spinal cord) takes origin from an elongated area of ectoderm, the neural plate, situated dorsally in the embryo, anterior to Hensen's node and primitive streak. The peripheral nervous system (PNS) arises from a specialized band of ectoderm, the neural crest, which flanks the lateral margins of the neural plate. In the development of the CNS, the neural plate assumes a major organizational role. By the 18th day of embryonic life, the edges of the neural plate become elevated forming the neural folds, with the depressed region intervening between folds constituting the neural grove (Figure 1). As development proceeds, the neural folds continue to elevate and sweeping medially, the opposing folds meet and fuse in the midline. This folding, with the resulting closure of the neural folds, thereby forms the neural tube. This closure of the neural folds with subsequent formation of the tube continues in a rostral and caudal direction. At the most rostral and caudal ends of this tube fusion is somewhat delayed. Thus continuity temporarily exists between the lumen of the neural tube and the surrounding amniotic fluid. The rostral and caudal poles of the neural tube at which point this continuity is established, are referred to as the anterior and posterior neuropores. Closure of the anterior neuropore occurs by the 23rd day, while the closure of the posterior neuropore lags until the 25th day. With the closure of the anterior and posterior neuropores the fundamental form of the human
2 CNS is that of a hollow tube. As the result of further differential growth and expansion of its walls, this tube can now be subdivided into an elongated caudal portion, which will become the spinal cord and a shorter, broader, cephalic part, the future brain, which early in its development appears as three dilations on the cephalic portion of the neural tube. II. Neural Tube: Caudal Neural Tube/Spinal Cord * Link to Netter Image 1.67 * Link to Netter Image 1.68 * Link to Netter Image 1.69 * Link to Netter Image 1.70 * Link to Netter Image 1.71 Histologic examination of the developing caudal neural tube reveals several interesting phenomena. During the neural plate stage and immediately after closure of the neural tube, the neural wall consists solely of neuroepithelial cells. With closure of the tube, some of these cells give rise to another cell type called a neuroblast, whose proliferation now causes distinct zonation within the neural tube. Those neuroepithelial cells from which the neuroblasts arose now constitute an inner zone, the ependymal layer which borders on the neural tube lumen. The migrating neuroblasts form an outer zone called the mantle layer which is destined to form the gray matter of the spinal cord, while proliferating nerve fibers originating from the neuroblasts constitute an outermost zone called the marginal layer, which is to become the white matter of the spinal cord.
3 Figure 1 Due to the continuous development of the neuroblasts and the subsequent formation of the mantle and marginal layers, several distinct changes are now noted in relation to the once simple caudal neural tube which is to form the spinal cord. Among these changes are the appearance of the: (Figure 2) 1. Alar plate - a dorsal thickening - future posterior (dorsal) horn 2. Basal plate - a ventral thickening - future anterior (ventral) horn 3. Sulcus limitans - a longitudinal furrow which marks the boundary between the sensory (alar) and motor (basal) portions of the central nervous system 4. Roof plate - thin dorsal midline portion of the neural tube - formed by ependymal and glial cells, it becomes a pathway for crossing or commissural fibers. 5. Floor plate - thin ventral midline portion of the neural tube - also pathway for crossing fibers 6. Ependymal lining - which has undergone a marked transition from its original stratified form 7. Neural crest development - these cells of neuroectodermal origin that appeared initially along the lateral edge of the neural plate now give rise to: a. Cell bodies of the dorsal root ganglia
4 b. Sympathetic ganglia cells c. Chromaffin cells (adrenal medulla) d. Neurilemmal (Schwann) cells e. Melanocytes f. Leptomeninges (pia and arachnoid) g. Cell bodies of the sensory ganglia of the 5th, 7th, 9th, and 10th cranial nerves - in relation to the rostral portion of the neural tube which is to become the brain. Figure 2 III. Malformations of the Caudal Neural Tube Spina bifida - This term covers a wide range of defects in which there is a failure of the dorsal portions of the vertebrae to fuse. (Figure 3)
5 Figure 3 1. Spinal bifida occulta-- Usually localized in the sacrolumbar region, and though there is a failure of the dorsal portions of the vertebral column to fuse, there is no protrusion of intraspinal contents to the surface. Figure 4
6 2. Meningocele -- The meninges of the spinal cord, bulge through the defect in the vertebral column, however, this developmental defect generally does not involve any neurological abnormalities. 3. Meningomyelocele -- Both the meninges and neural elements bulge through the defect in the vertebral column. Figure 5 4. Complete Rachischisis -- The neural tube remains unclosed and the defective spinal cord lies exposed on the infant's back. 5. Congenital dermal sinus -- Represents the remnants of an incomplete cleavage of the cutaneous and neural ectoderm during embryonic life. There is usually a narrow opening appearing as a small dimple in the midline and a tract lined with stratified squamous epithelium. IV. Neural Tube: Rostral Portion/Brain (General Features) * Link to Netter Image 1.73 * Link to Netter Image 1.74 The rostral portion of the neural tube terminates as the lamina terminalis representing the
7 closure of the anterior neuropore. This region divides into three primary vesicles which by the third week of life are termed from rostral to caudal, the prosencephalon, mesencephalon, and rhombencephalon. By the fifth week of life, these three primary vesicles undergo dramatic transformation with the rostral prosencephalic bulge differentiating into two telencephalic bulges, capping a relatively undifferentiated midline bulge termed the diencephalon (Figure 4). The intermediate bulge, the mesencephalon, remains relatively undifferentiated, while the caudal bulge, the rhombencephalon further differentiates into the rostral metencephalon and the more caudally directed myelencephalon which is confluent with the spinal cord (Figure 4). Although this basic developmental pattern of the rostral neural tube is relatively straightforward, the actual alignment of these primary brain vesicles is somewhat difficult to conceptualize. This is due to the fact that, as the rostral portion of the neural tube develops, it undergoes extreme flexuring, with compensatory infolding. Thus, in the early gestational period, the ventral surface of the mesencephalon shows an infolding, termed the mesencephalic or cephalic flexure, while a comparable ventral infolding forms at the junction of the myelencephalon and spinal cord, termed the cervical flexure. These ventrally originating flexures are compensated, in part, by the development of a dorsal infolding between the mesencephalon and myelencephalon termed the pontine flexure. Figure 6
8 In relation to the developing brain and brain stem, the mesencephalon, metencephalon, and myelencephalon follow a development pattern quite reminiscent of that seen in the spinal cord, whereas the diencephalic and telencephalic regions deviate from this developmental plan. Specifically: A. In relation to the brain stem, the spinal cord patterns of alar and basal plates persist throughout the myelencephalon, metencephalon and mesencephalon, with a major distinction involving the expansion or closure of the roof plate. As can be seen in Figure 5, the basal plate, as in the spinal cord, gives rise to motor neurons that are organized in discrete columns reflecting specific the functional components of the cranial nerves with which they are associated. For example, the most medial column contains cells contributing to general somatic efferent functional components of the cranial nerves, while the intermediate and more lateral basal columns provide for the special visceral efferent and general visceral efferent functional components respectively. Figure 7
9 The alar plate gives rise to sensory neurons which are also organized in distinct columns, again reflecting the specific functional components of those cranial nerves with which they are associated. The most medial column of neurons is associated with general visceral afferents, while the intermediate and lateral columns are associated with special visceral afferents and general and special somatic afferents respectively. In addition to providing for these sensory columns, the alar plate of the brain stem also contributes some migratory cells which give rise to cell groups or clusters scattered throughout the ventral brain stem. Lastly, in the process neural development, the marginal zone undergoes significant expansion and modification due to the presence of large numbers of ascending and descending fiber systems which, in concert with the development of local nuclear groups, give the brain stem its characteristic shape, particularly in the ventral region. B. In relation to the diencephalon and telencephalon, these regions spring exclusively from the alar plate, and thus, undergo developmental patterns quite dissimilar seen in the brain stem and spinal cord. V. Rostral Neural Tube - Specific Developmental Features of the Brain Stem A. Myelencephalon (Figure 8) 1. Although following the organizational plan seen in the developing spinal cord, the developing myelencephalon or medulla undergoes a dramatic thinning of the roof plate so that alar plates migrate laterally and the basal plates shift to a midline position. The thinned roof plate covers a large fluidfilled chamber which will persist as the fourth ventricle. Further, thinning in the mid and lateral quadrants of the roof plate will give rise to foramina of Magendie and Luschka respectively, whereas the ingrowth of pial and mesenchymal tufts give rise to the choroid plexus of the fourth ventricle. 2. The basal plate gives rise to all the motor neurons of the medullary region with the general somatic efferent cell clusters giving rise to the hypoglossal nucleus, the special visceral efferent cell clusters giving rise to the nucleus ambiguus, and the general visceral efferent cell clusters giving rise to the dorsal motor nucleus of the vagus. 3. As previously noted, the alar plate will differentiate into the sensory components of the medulla, with the medial and intermediate cell groupings giving rise to the nucleus solitarius. The more lateral cell groupings give rise to the vestibular nuclei as well as the gracile and cuneate nuclei. In addition to forming the sensory columns, the alar plate also gives rise to a thin, ventrally directed stream of neurons which forms the bulbopontine extension. These migrating cells form the inferior olivary nucleus and continue rostrally to contribute to the formation of some of the caudal pontine nuclei.
10 4. The ventrally lying marginal zone which encompasses both the basal and alar plates initially shows little overt change; however, over time its shape is altered by the continuing expansion of the inferior olivary nuclei as well as the presence of large numbers of ascending and descending fiber systems. This region undergoes further change as these ascending and descending systems undergo myelination. Typically, by the sixth month, this region shows myelination within the medial longitudinal fasciculus, soon followed by myelination of the vestibulospinal, reticulospinal, and tectospinal tracts. Afferent fibers are not myelinated until the eighth fetal month, when the corticospinal system also undergoes myelination. Figure 8 B. Metencephalon (Figure 8)
11 1. In general, the metencephalon replicates many of the important features seen in the myelencephalon. Initially, the roof plate of the metencephalon is thin. It is triangular in shape, with the apex of the triangle situated cranially. The alar plates of this part of the developing brain approach each other as they are traced forward, the most dorsal portions of the alar plates undergo thickening to form the primordium of the cerebellum discussed below. The ventral medial portion of the alar plate forms the pontine component of the bulbopontine extension which helps seed the pontine nuclei. A portion of the ventral medial plate not undergoing migration gives rise to the somatic afferent nuclei. In this regard, the caudal portion of the alar plate forms the somatic afferents of the vestibular and cochlear nuclei, whereas the more cranial portion of this mass gives rise to the general somatic afferents of the chief sensory nucleus of V. 2. Cerebellum The cerebellum originates from the dorsal portion of the alar plate termed the rhombic lip. Initially, the rhombic lips from both sides of the metencephalon grow into the ventricular compartment, merging in the midline, forming a continuous cerebellar primordium. Once this fusion is complete, the cerebellum undergoes expansion of its extraventricular portion. 3. In the developing basal plate of the metencephalon, one can find motor columns comparable to those found in the basal plate of the myelencephalon. Again, these motor columns are highly organized, with the most medial cell clusters giving rise to general somatic efferents such as the abducens nucleus, which the more lateral cell columns give rise to the special visceral efferents of the facial nucleus and motor nucleus of V. The most lateral cell column gives rise to the general visceral efferents associated with the superior salivatory nucleus and perhaps inferior salivatory nucleus. 4. Like the myelencephalon, the metencephalon undergoes further expansion of the marginal zone due to the ingrowth of afferents and efferents as well as ongoing myelination. The pontine nuclei contribute to further expansion in that they give rise to the transverse pontine fibers which stream into the cerebellum, contributing to the formation of the massive middle cerebellar peduncle. C. Mesencephalon 1. The mesencephalon closely replicates many of the developmental features seen in the developing spinal cord. The alar plates differentiate into the sensory domains of the superior and inferior colliculi involved with the visual and auditory pathways respectively. The underlying ventricular space becomes narrowed, much like the central canal, forming the cerebral aqueduct which is the conduit between the third and fourth ventricle. 2. The developing basal plates, as in the other brain stem regions, give rise to motor nuclei. Once again, the most medial of the motor columns give rise to the general
12 somatic efferent components of the oculomotor and trochlear nerves, while the more lateral of the motor columns gives rise to the Edinger-Westphal nucleus. 3. The origin of the red nucleus and substantia nigra are controversial. Some contend that both of these nuclear groups derive from the alar plate, while others argue that these nuclei develop in situ in the basal plate itself. 4. The marginal zone undergoes characteristic expansion due to the presence of large numbers of descending corticospinal, corticobulbar, and corticopontine projections which expand marginal zone bilaterally resulting in the development of the characteristic cerebral peduncles. VI. Rostral Neural Tube - Specific Developmental Features of the Forebrain * Link to Netter Image 1.75A * Link to Netter Image 1.75B * Link to Netter Image 1.75C * Link to Netter Image 1.75D * Link to Netter Image 1.75E * Link to Netter Image 1.75F * Link to Netter Image 1.76 As was noted, the forebrain is derived from the prosencephalic bulge which further subdivides into two telencephalic swellings that expand around a centrally directed diencephalon. A. Diencephalon 1. Early in the development of the alar plate in this region, the hypothalamic sulcus is formed, separating the thalamus from the hypothalamus. This sulcus, in turn, is followed by the development of another sulcus, the epithalamic sulcus, which isolates the dorsal thalamus proper from the overlying epithalamic domain. Cells within the mantle zone of the epithalamic region differentiate into the habenular nuclei which lies adjacent to the pineal stalk. The stria medullaris thalami also develops in this region which undergoes relatively regressive growth in comparison to the underlying thalamus. Thus, in the adult man, the epithalamus is proportionally smaller than the underlying thalamus. 2. In the hypothalamic region, neuroblasts within the mantle zone differentiate into various nuclei associated with visceral function. In the thalamic region, nuclei within the mantle zone and those migrating into the marginal zone develop into the thalamic nuclei proper in addition to the metathalamic nuclei, the medial and lateral geniculate bodies. With expansion of these nuclei, the thalamus swells and projects medially where it compresses the third ventricular cavity. In some cases, portions of these thalamic swellings fuse in the midline, giving rise to the mass intermedia or interthalamic
13 adhesion. 3. The roof plate of the diencephalon is thin and is invaginated by pial elements which form the tela choroidea with the subsequent formation of the choroid plexus of the third ventricle. In the posterior aspect of the roof of the diencephalon, an outgrowth arises which extends upward and forward as a hollow mass. Over time, this hollow mass becomes filled with proliferating cells which transform this projection into the pineal gland. 4. A medium diverticulum in the floor plate forms the neurohypophysis which is encompassed by the adenohypophysis that arises from the roof plate. B. Telencephalon 1. General Developmental Features - The telencephalic vesicles arise during the seventh week of development as outgrowths of the prosencephalic cavity. Initially, these outgrowths exist as relatively thin bands of tissue surrounding relatively massive ventricular cavities which are confluent with the third ventricle through the interventricular foramina. The interventricular foramina are bounded anteriorally by the lamina terminalis which delineates the closure of the anterior neuropore. Initially, the telencephalic bulges lie posterior and lateral to the lamina terminalis; however, over time, both telencephalic bulges expand, moving rostrally, superiorally, posteriorally and inferiorally. With rapid telencephalic growth, large numbers of neuroblasts migrate through the mantle layer to the outer marginal zone, where they form the cerebral cortex or pallium. The growth pattern of the pallium is planar, growing rapidly as an expanding two-dimensional sheet. In the ventral portion of the telencephalon, the basal ganglia arise from the mantle zone. As a result of differential growth patterns, the pallium expands like the shell of a balloon. At the same time, the rapidly growing basal ganglia push into the balloon like an expanded fist. As result of this process, the basal ganglia expand into the ventricle from the ventral medial aspect of the telencephalon and the pallium balloons outward, forward, and to the rear, while that portion of the pallium directly related to the basal ganglia undergoes little expansion. In fact, it is this process that results in the differential development of the frontal, parietal, temporal and occipital lobes which will balloon out and encompass the insular lobe which is held in place by the developing basal ganglia. 2. Specific Development of the Pallium (Figure 7) Over time, the developing pallium becomes organized into archipallium which is confined to the dorsal midline, the paleopallium, which is located more ventrally and the neopallium which spans the areas between these two regions, giving rise to the bulk of the convexity of the cerebral cortex. As the development proceeds, the neopallium grows at a fast rate, and both the archipallium and paleopallium are displaced to more medial positions.
14 (Figure 8) a. The archipallium which gives rise to the hippocampal formation is displaced in a caudal direction into the medial wall of the temporal lobe, due to the extensive growth of the neopallium in both the frontal and lateral areas. b. The pyriform and entorhinal cortices, which are parts of the paleopallium, are displaced medially and inferiorally to the basal portion of the temporal lobe. The neopallium undergoes major expansion which persists as the bulk of the definitive cerebral cortex. c. Initially, all areas of the cerebral cortex appear smooth, showing no gyri and sulci. With continued development, however, gyri and sulci develop so that by birth the lissencephalic brain is transformed into a brain containing the complex gyri and sulci. Figure 9 3. Commissural Fibers (Figure 10) With the growth of the cerebral hemispheres, there is a concomitant development of the major commissural systems, all of which derive from portions of the lamina terminalis. Although the specific origin of these pathways is somewhat
15 controversial, it appears that the anterior commissure and hippocampal commissure are the first to appear, followed in the tenth week of gestation by the development of the corpus callosum. Lastly, the posterior commissure as well as the optic chiasm appear. Figure Corpus striatum - Basal Ganglia (Figure 11) As noted, the basal ganglia are derived from the base of the telencephalon and protrude into the forming ventricular cavity. Initially, due to marked proliferation in the mantle zone of this region, the basal ganglia differentiate into medial and lateral striatal elevations. With expansion of the cerebral hemispheres, these striatal elevations form longitudinal ridges in the floor of the main part of the
16 ventricular cavity, and when traced caudally, lie in the anterior wall of the descending portion of the ventricle and the roof of the inferior horn. These relationships are attributed to the fact that the striatal development proceeds in relation to the expanding and turning cerebral hemispheres. In general, ascending and descending cortical fibers further divide these bulges into a dorsal medial portion which forms the caudate and a dorsal lateral portion which forms the putamen and globus pallidus. The descending and ascending cortical fibers involved in this process form the internal capsule. Figure 11 VI. Abnormal Development of the Brain As one can imagine the complex processes described above suggests the potential for various forms of congenial abnormality. While the purpose of this lecture is not to provide detailed insight into the neurobiology of all CNS developmental abnormalities, the following are provided to give examples of some of the key developmental abnormalities
17 that can occur. 1. Marked disorders of neurulation can occur with non-closure of the anterior neuropore. The common abnormalities related to this include complete dysaphia, anencephaly, exencephaly, and Meningoencephalocele. These malformations are recognized as direct failures of neurulation since CNS tissue is directly exposed to the outside of the body. In anencephaly, most of the frontal and parietal bones are absent with the forebrain appearing as a hemorrhagic mass. Exencephaly involves a condition in which the brain is outside of the skull and Meningoencephalocele involves the herniation of both brain and meningeal tissue out through a defect in the skull. Figure 12 Figure 13
18 2. Developmental Abnormalities Associated with the Forebrain a. Pachygyria, a condition which the gyri are abnormally broad. b. Lissencephaly - a condition in which there is a virtual absence of gyri and sulci Figure 14 c. Microgyri - refers to a reduction in the size of the gyri d. Hydranencephaly - a condition associated with virtual resorption of all the telencephalic mass, such that the telencephalon persists as a thin strand of tissue encompassing grossly enlarged ventricular cavities. e. Porencephaly - involves the destruction of specific areas of the cortices, resulting in a direct conduits established between the ventricular and cerebrospinal fluid fronts. Figure 15
19 3. Agenesis Development can be associated with the absence or agenesis of various parts of the brain including a. Agenesis of the corpus callosum Figure 16 b. Agenesis of the cerebellar hemispheres c. Agenesis of the cerebellar vermis * Netter Presenter Image Copyright 2004 Icon Learning Systems. All rights reserved.
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