Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium

Various lines of evidence suggest that the development and evolution of the mammalian isocortex cannot be easily explained without an understanding of correlative changes in surrounding areas of the telencephalic pallium and subpallium. These are close neighbours in a common morphogenetic field and are postulated as sources of some cortical neuron types (and even of whole cortical areas). There is equal need to explain relevant developmental evolutionary changes in the dorsal thalamus, the major source of afferent inputs to the telencephalon (to both the pallium and subpallium). The mammalian isocortex evolved within an initially small dorsal part of the pallium of vertebrates, surrounded by other pallial parts, including some with a non-cortical, nuclear structure. Nuclear pallial elements are markedly voluminous in reptiles and birds, where they build the dorsal ventricular ridge, or hypopallium, which has been recently divided molecularly and structurally into a lateral pallium and a ventral pallium. Afferent pallial connections are often simplified as consisting of thalamic fibres that project either to focal cell aggregates in the ventral pallium (predominant in reptiles and birds) or to corticoid areas in the dorsal pallium (predominant in mammals). Karten's hypothesis, put forward in 1969, on the formation of some isocortical areas postulates an embryonic translocation into the nascent isocortex of the ventropallial thalamorecipient foci and respective downstream ventropallial target populations, as specific layer IV, layers II- III, or layers V-VI neuron populations. This view is considered critically in the light of various recent data, contrasting with the alternative possibility of a parallel, separate evolution of the different pallial parts. The new scenario reveals as well a separately evolving tiered structure of the dorsal thalamus, some of whose parts receive input from midbrain sensory centres (collothalamic nuclei), whereas other parts receive oligosynaptic 'lemniscal' connections bypassing the midbrain (lemnothalamic nuclei). An ampler look into known hodological patterns from this viewpoint suggests that ancient collothalamic pathways, which target ventropallial foci, are largely conserved in mammals, while some emergent cortical connections can be established by means of new collaterals in some of these pathways. The lemnothalamic pathways, which typically target ancestrally the dorsopallial isocortex, show parallel increments of relative size and structural diversification of both the thalamic cell populations and the cortical recipient areas. The evolving lemnothalamic pathways may interact developmentally with collothalamic corticopetal collaterals in the modality-specific invasion of the emergent new areas of isocortex.     

Primary retinal targets in the Atlantic loggerhead sea turtle,Caretta caretta

Summary Autoradiographic analysis distinguished twelve primary retinal targets in the diencephalon and the mesencephalon of the Atlantic loggerhead sea turtle, Caretta caretta. While the majority of fibers terminate contralaterally, sparse labelling is seen over ipsilateral thalamic nuclei. The dorsal optic nucleus is the most expansive retinal target in the dorsal thalamus. Four nuclei ventral and one dorsal, to the dorsal optic nucleus, receive retinal input. Before terminating in the optic tectum, labelled fibers pass through the pretectum terminating in four nuclei. Within the superficial zone of the optic tectum, three terminal zones are recognized. A distinct accessory tegmental tract separates from the main optic tract terminating in the basal optic nucleus.While such a multiplicity of retinal targets occurs among other reptiles, birds and mammals, it is presently impossible to accurately recognize visual homologies among amniotic vertebrates.     

The effect of bicuculline on behavior and on the neuronal activity of the caudate nucleus and of the thalamic VA-VL nuclei in the cat brain]

In chronic cat experiments, bicucullin-induced GABA receptor blockade in the dorsal and ventral parts of the rostral caudate nucleus resulted in complicated changes in spontaneous activity of 19 of 55 neurons, primarily in the cells with low spike frequency. Changes were observed also in 8 to 31 neurons of VA-VL nuclei of the thalamus. The blockade of striatal GABA receptors was accompanied by changes in motor behavior and emotional motivational state of the animals. The character and latency of unit activity rearrangements in the caudate nucleus and modifications of cat's behavior depended on the localization of bicucullin injection point within different parts of the caudate nucleus.     

A comparison of microdistributions of taurine and cysteine sulphinate decarboxylase activity with those of GABA and L-glutamate decarboxylase activity in rat spinal cord and thalamus

Abstract— Distribution profiles of taurine and activity of cysteine sulphinate decarboxylase (CSD), the enzyme catalysing the formations of hypotaurine from cysteine sulphinate and of taurine from cysteate respectively, in the rat spinal cord and thalamus were studied in comparison with those of GABA and activity of l -glutamate decarboxylase (GAD), the rate limiting enzyme for GABA formation. In the spinal cord (L₂-L₃), it was found that taurine is fairly evenly distributed, whereas the activity of CSD is higher in the dorsal half of the spinal cord than in the ventral half. The highest CSD activity was found in the dorsal part of the dorsal horn. In the anterior part (A 5.4) of the thalamus, taurine and CSD activity were also distributed evenly and no areas having high taurine content and CSD activity were detected. In contrast with the even distributions of taurine and CSD activity, both GABA and GAD activity were distributed unevenly in the same CNS areas examined: The areas having high GABA content and GAD activity in the thalamus (A 5.4) coincided with the ventrolateral part of the ventral nucleus of thalamus (VM), entopeduncular nucleus (EP) and nucleus reuniens thalami (RE), whereas those in the spinal cord were found to be in the dorsal part of the dorsal horn and surrounding parts of the central canal, respectively. Considering a probable role of GABA in mammalian central nervous system (CNS) as an inhibitory neurotransmitter, it seems unlikely that taurine acts as an inhibitory neurotransmitter at least in the rat spinal cord and thalamus.     

Electrophysiological analysis of the organization of somatosensory thalamic inputs in the frog

Potentials produced in the frog thalamus by electrical stimulation of the peripheral nerves were investigated by sink and current source-density analysis. Sinks, which are viewed as potential generation sites, were located in three regions: the cell-free zone of the ventral thalamus adjoining the ventrolateral nucleus, the ventromedial and ventrolateral nuclei, and the caudal section of the dorsal thalamus. Evoked activity was recorded in individual neurons in the area of the second and third of these sinks. The first sink failed to form after section of the dorsal tracks of the spinal cord, while the remaining two only appeared after a considerably extended latency. It is suggested that nuclei of the ventral and caudal sections of the dorsal thalamus receive somatic impulses through the systems connected with the dorsal as well as the ventrolateral columns of the spinal cord. The direct projections of the primordial nuclei of dorsal columns may be involved in afferentation the ventral thalamus.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 18, No. 5, pp. 687–695, September–October, 1986.     

Dorsal thalamic connections of the ventral lateral geniculate nucleus of rats

In order to understand better the organisation of the ventral lateral geniculate nucleus of the ventral thalamus, this paper has examined the patterns of connections that this nucleus has with various nuclei of the dorsal thalamus in rats. Injections of biotinylated dextran or cholera toxin subunit B were made into the parafascicular, central lateral, posterior thalamic, medial dorsal, lateral dorsal, lateral posterior, dorsal lateral geniculate, anterior, ventral lateral, ventrobasal and medial geniculate nuclei of Sprague-Dawley rats and their brains were processed using standard tracer detection methods. Three general patterns of ventral lateral geniculate connectivity were seen. First, the parafascicular, central lateral, medial dorsal, posterior thalamic and lateral dorsal nuclei had heavy connections with the parvocellular (internal) lamina of the ventral lateral geniculate nucleus. This geniculate lamina has been shown previously to receive heavy inputs from many functionally diverse brainstem nuclei. Second, the visually related dorsal lateral geniculate and lateral posterior nuclei had heavy connections with the magnocellular (external) lamina of the ventral lateral geniculate nucleus. This geniculate lamina has been shown by previous studies to receive heavy inputs from the visual cortex and the retina. Finally, the anterior, ventral lateral, ventrobasal and medial geniculate nuclei had very sparse, if any, connections with the ventral lateral geniculate nucleus. Overall, our results strengthen the notion that one can package the ventral lateral geniculate nucleus into distinct visual (magnocellular) and non-visual (parvocellular) components.     

Distribution of trigeminothalamic and spinothalamic lamina I terminations in the cat

The distribution in the thalamus of terminal projections from lamina I neurons of the trigeminal, cervical, and lumbosacral dorsal horn was investigated with the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L) in the cat. Iontophoretic injections were guided by single- and multi-unit physiological recordings. The injections in particular cases were essentially restricted to lamina I, whereas in others they spread across laminae I–III or laminae I–V. The trigemino- and spinothalamic (TSTT) terminations were identified immunohistochemically. In all cases, regardless of the level of the injections, terminal fibers were consistently distributed in three main locations: the submedial nucleus; the ventral aspect of the basal ventral medial nucleus and ventral posterior nuclei; and, the dorsomedial aspect of the ventral posterior medial nucleus. The terminal fields in the submedial nucleus and the ventral aspect of the ventral posterior group were topographically organized. Terminations along the ventral aspect of the ventral posterior group extended posterolaterally into the caudal part of the posterior nucleus and anteromedially into the ventromedial part of the ventral lateral nucleus. In several cases with trigeminal lamina I injections, a terminal labeling patch was observed within the core of the ventral posterior medial nucleus. In cases with spinal lamina I injections, terminations were also consistently found in the lateral habenula, the parafascicular nucleus, and the nucleus reuniens. Isolated terminal fibers were occasionally seen in the zona incerta, the dorsomedial hypothalamus, and other locations. These anatomical observations extend prior studies of TSTT projections and identify lamina I projection targets that are important for nociceptive, thermoreceptive, and homeostatic processing in the cat. The findings are consistent with evidence from physiological (single-unit and antidromic mapping) and behavioral studies. The novel identification of spinal lamina I input to the lateral habenula could be significant for homeostatic behaviors.     

Identification of tuberculo-ventral neurons in the polymorphic layer of the rat dorsal cochlear nucleus

The tuberculo-ventral tract represents a short nervous circuit within the auditory cochlear nuclei. Tuberculo-ventral neurons of the dorsal cochlear nucleus send isofrequency inhibitory inputs to bushy cells of the ventral cochlear nucleus. Injection of wheat germ agglutinin conjugated to horseradish peroxidase into the rat ventral cochlear nucleus, labelled tuberculo-ventral neurons retrogradely in the deep polymorphic layer of the ipsilateral dorsal cochlear nucleus. Five to 20% of the perimeter of these cells was covered by synaptic boutons, most of which contained flat and pleomorphic vesicles. These boutons contained glycine and sometimes GABA. Occasional small axo-somatic boutons contained round vesicles and were immunonegative for both glycine and GABA. This study shows that the synaptic profile of tuberculo-ventral neurons is different from that of other medium-size glycinergic neurons within the polymorphic layer or more superficial regions of the dorsal cochlear nucleus like cartwheel neurons. In fact the latter mostly receive boutons that contain pleomorphic vesicles.     

Afferent connections of the basolateral division of the amygdaloid complex of the cat brain

Injection of horseradish peroxidase into the basal macrocellular and lateral nuclei of the amygdaloid complex (BLAC) in the cat brain has revealed their rich thalamic afferentation. On the BLAC there are massive projections of: a) nuclei of the middle line of the precommissural pole of the dorsal thalamus (anterior parts of the paratenial, interanteromedial and reunial nuclei), as well as the whole anterior paraventricular nucleus, medial part of the ventral posteromedial nucleus; b) postcommissural nuclei of the dorsal thalamus; some "nonacustical" nuclei of the internal geniculate body (ventrolateral nucleus, medial and macrocellular parts and the most caudal end of the internal geniculate body). Rather essential are projections of the "posterior group nuclei", those of the suprageniculate nucleus, of some parts of the ventral thalamus (subparafascicular nucleus, marginal and peripeduncular nuclei) and parabrachial nucleus. Scattered single projections are obtained from all hypothalamic parts (most of all the ventromedial nucleus), reticular nuclei of the septum, substantia innominata, substantia nigra, truncal nuclei of the raphe. Variety of the dorsal thalamic nuclei, sending their fibers to the BLAC reflects variety of sensory information, that gets here, according to its modality, degree of its differentiation and integrity. A number of the dorsal thalamus nuclei, owing to abundance of labelled neurons, can be considered as special relay thalamic nuclei for the BLAC resembling corresponding relay nuclei for the new cortex.     

Topography of retinal axons in the diencephalon of goldfish

Summary The projections of horseradish peroxidase-filled axons from each quadrant of the retina were studied to determine whether retinal projections of goldfish are topographically organized in diencephalic target nuclei. A distinct topography of the dorsal, nasal, ventral and temporal retina exists in the lateral geniculate nucleus and in the dorsolateral optic nucleus of the thalamus. The projections of retinal quadrants show minimal spatial overlap in each of these nuclei. The suprachiasmatic nucleus of the hypothalamus is extensively innervated by ventral retinal fibers, whereas the nucleus is sparsely innervated by fibers from the other three retinal quadrants. A rudimentary topography also exists in the pretectum where the dorsal pretectal area receives projections primarily from the ventral retina and the ventral pretectal area receives projections mostly from the dorsal retina. These data show that retinal projections to some diencephalic nuclei are topographically organized.This work was supported by Research Grant EY-01426 to S.C.S.     

MEASUREMENT OF γ-AMINOBUTYRIC ACID IN ISOLATED NERVE CELLS OF CAT CENTRAL NERVOUS SYSTEM

Abstract— A sensitive method for measuring γ-aminobutyric acid (GABA) has been developed. This method consists of a combination of the enzymic GABA assay of J akoby and S cott (1959) with the enzymic cycling technique of L owry , P assonneau , S chulz and R ock (1961) and permits the measurement of as little as 2 × 10⁻¹⁴ mol of GABA. Using this method, GABA analyses were made on single isolated nerve cell bodies of different types from the CNS of the cat. Average GABA concentrations in these cell bodies were: spinal ganglion cells, 0.2 m m ; spinal mononeurons, 0.9 m m ; large cells of the ventral part of Deiters' nucleus, 2.7 m m ; large cells of the dorsal part of Deiters' nucleus, 6.3 m m ; cerebellar nuclei cells, 6.0 m m ; cerebellar Purkinje cells, 6.6mM; cerebral Betz cells, 2.5 m m .
The GABA concentrations in the isolated dorsal Deiters' cells were greatly reduced (1.7 m m ) after the removal of the cerebellar vermis while those of the ventral Deiters' cells were unaffected by the denervation. These results suggest that GABA is concentrated within axon terminals, probably of Purkinje neurons, synapsing with the dorsal Deiters' cells. The results of GABA analyses on isolated nerve cells are discussed in relation to the relevant neuronal functions and the possible role of GABA as an inhibitory transmitter.     

The cochlear nuclei in man.

The human cochlear nuclei are composed of a ventral and a dorsal nucleus which are similar, though not identical, in their cytoarchitecture to those of other mammals. The ventral cochlear nucleus (VCN) consists of a rostral area of spherical cells, a central area of multipolar and globular cells, a posterior area of octopus cells, and laterodorsal cap of small neurons. The interareal boundaries are less distinct in man than in the cat. The central region of multipolar cells and the cap area of small cells constitute the bulk of the human VCN. The spherical, globular, and octopus cells appear relatively less numerous in man than in other mammals. The dorsal cochlear nucleus (DCN) in man is relatively large, but lacks the typical stratification seen in other mammals, with only vestiges of the granular and molecular layers remaining. Virtually the entire DCN consists of an area of cochlear fiber neuropil containing pyramidal cells, small neurons, and occasional giant cells. The pyramidal cells have lost their typical radial orientation and lie scattered within the cochlear neuropil. Thus the entire human DCN may be equivalent to layers 2 and 3 of this nucleus in other mammals. In spite of the relatively large DCN, the acoustic striae appear small. This is in contrast to the large trapezoid body leaving the VCN. Intrinsic and descending fiber pathways to the cochlear nuclei are not clearly defined and may be less prominent in man than in the cat.     

Thalamocortical axons are influenced by chemorepellent and chemoattractant activities localized to decision points along their path

Thalamocortical axons (TCAs), which originate in dorsal thalamus, project ventrally in diencephalon and then dorsolaterally in ventral telencephalon to their target, the neocortex. To elucidate potentially key decision points in TCA pathfinding and hence the possible localization of guidance cues, we used DiI-tracing to describe the initial trajectory of TCAs in mice. DiI-labeled TCAs extend ventrally on the lateral surface of ventral thalamus. Rather than continuing this trajectory onto the lateral surface of the hypothalamus, TCAs make a sharp lateral turn into ventral telencephalon. This behavior suggests that the hypothalamus is repulsive and the ventral telencephalon attractive for TCAs. In support of this hypothesis, we find that axon outgrowth from explants of dorsal thalamus is biased away from hypothalamus and toward ventral telencephalon when cocultured at a distance in collagen gels. The in vivo DiI analysis also reveals a broad cluster of retrogradely labeled neurons in the medial part of ventral telencephalon positioned within or adjacent to the thalamocortical pathway prior to or at the time TCAs are extending through it. The axons of these neurons extend into or through dorsal thalamus and appear to be coincident with the oppositely extending TCAs. These findings suggest that multiple cues guide TCAs along their pathway from dorsal thalamus to neocortex: TCAs may fasciculate on the axons of ventral telencephalic neurons as they extend through ventral thalamus and the medial part of ventral telencephalon, and chemorepellent and chemoattractant activities expressed by hypothalamus and ventral telencephalon, respectively, may cooperate to promote the turning of TCAs away from hypothalamus and into ventral telencephalon.     

Morphological characteristics of different types of neurons in the ventrooralis anterior,ventrooralis internus,and ventrooralis posterior nuclei in the human thalamus

1. Golgi-Kopsch preparations of the oral ventral nuclei of human thalamus were analyzed in an attempt to classify the neuronal types. 2. Three types of neurons are described for the first time in humans. Type I neurons are large or medium in size and bear dendrites with protrusions, spines, and short hair-like appendages. Some have a radiate dendritic arbor and others have dendrites grouped in tufts. The dendritic trees of these neurons are dense. 3. Type II neurons are medium or small in size with less dense dendritic trees. These cells have somatic as well as dendritic appendages of different forms. 4. Relatively rare is a type of very small neurons, type III, with few and sparsely branching dendrites.     

Somatotopic organization and cortical projections of the ventrobasal complex of the flying fox: an "inverted" wing representation in the thalamus

The present study investigates the somatotopic representation in the somatosensory thalamus of a megachiropteran bat. Using standard microelectrode mapping techniques, representational maps were generated for the ventrobasal (Vb) and posterior (Po) thalamic complexes of the Grey-headed flying fox. Anatomical tracing from neocortical injections provided additional data confirming the somatotopy found physiologically. A full representation of the body surface innervated by the trigeminal and spinal nerves was found. However, in contrast with other mammals, the representations of the forelimb and adjacent thoracic trunk within the thalamus were inverted. This means that the distal portions of the wing membrane and the tips of the digits were represented dorsally in Vb, and the thoracic trunk was represented ventrally. In Po the digit tips were represented in the ventral most portion and the thoracic trunk in the dorsal portion of the nucleus. These results are discussed in relation to similarities of megachiropteran somatosensory thalamic nuclei to those of other mammalian species and in relation to the formation of thalamic somatotopic maps and fiber sorting.     

Somatotopic organization and cortical projections of the ventrobasal complex of the flying fox: an "inverted" wing representation in the thalamus

The present study investigates the somatotopic representation in the somatosensory thalamus of a megachiropteran bat. Using standard microelectrode mapping techniques, representational maps were generated for the ventrobasal (Vb) and posterior (Po) thalamic complexes of the Grey-headed flying fox. Anatomical tracing from neocortical injections provided additional data confirming the somatotopy found physiologically. A full representation of the body surface innervated by the trigeminal and spinal nerves was found. However, in contrast with other mammals, the representations of the forelimb and adjacent thoracic trunk within the thalamus were inverted. This means that the distal portions of the wing membrane and the tips of the digits were represented dorsally in Vb, and the thoracic trunk was represented ventrally. In Po the digit tips were represented in the ventral most portion and the thoracic trunk in the dorsal portion of the nucleus.These results are discussed in relation to similarities of megachiropteran somatosensory thalamic nuclei to those of other mammalian species and in relation to the formation of thalamic somatotopic maps and fiber sorting.     

Lamination of spinal cells projecting to the zona incerta of rats

In this study, the lamination patterns of spinal cells projecting to the zona incerta (ZI), intralaminar nuclei and ventral posterior nucleus of the thalamus have been explored. Injections of cholera toxin subunit B or latex beads were made into the ZI, intralaminar and ventral posterior nuclei of Sprague Dawley rats. The brain and spinal cord were then aldehyde fixed and processed using standard methods. Our results show two major findings. First, after injections into the ZI, there is a distinct pattern of lamination of labelled cells in the spinal cord, a pattern that changes across the different levels. At cervical levels, labelled cells are located within the medial region of the deep dorsal horn, while at lumbar and sacral levels, they are found in the intermediate grey matter. These results are similar to those seen after injections into the intralaminar or ventral posterior nuclei, except that in the latter cases, more labelled cells are located in the superficial laminae of the dorsal horn, particularly from the ventral posterior nucleus. Second, the ZI is not associated uniformly with all spinal levels; labelling is heaviest at cervical and lightest at thoracic levels. From each thalamic injection site, labelling is noted on both sides of the spinal cord, with a clear contralateral predominance. In conclusion, the results indicate that the ZI receives a distinct set of spinal projections principally from the cervical level. The particular pattern of lamination of spinal cells projecting to the ZI suggests that the type of information relayed is from deep somatic and/or visceral structures, and probably nociceptive in nature.     

Gene mapping in marsupials and monotremes, V. Synteny between hypoxanthine phosphoribosyltransferase and phosphoglycerate kinase in the platypus

In order to extend comparative mapping studies to the monotreme mammals (subclass Prototheria), somatic-cell hybrids were obtained between Chinese-hamster cells deficient in hypoxanthine phosphoribosyltransferase (HPRT) and platypus fibroblasts. The characteristics of these hybrids closely resemble those of metatherian x eutherian hybrids, in that they are recovered at low frequency and they rapidly segregate and fragment platypus chromosomes. Biochemical and cytological studies of the hybrids, their subclones and HPRT-deficient revertants indicate that phosphoglycerate kinase is syntenic with HPRT in the platypus (as it is in other mammals); however, the studies do not permit chromosomal assignment of the syntenic group. The implications of the chromosomal location of this ancient synteny group for the evolution of the mammalian X chromosome are discussed.     

Development and evolution of thalamocortical interactions

Thalamocortical projections in mammals must travel through a considerable portion of the newly formed subdivisions of the embryonic forebrain. They descend through the ventral thalamus, advance in the internal capsule amongst cells which already possess dorsal thalamic projections, traverse the striatocortical junction, and then reach the cerebral cortex by associating with subplate cells and their early corticofugal fibers. The interactions of the thalamocortical projections with early generated, largely transient cells of these regions are believed to play a crucial role in their deployment. These ideas are supported by recent work on reeler and other strains of mutant mice. While we are beginning to understand the basic pattern of the cellular and molecular interactions employed in mammalian thalamocortical development, comparative developmental studies hold the promise to reveal the underlying logic of these steps and the evolutionary origin of the mammalian cerebral cortex.