Plasticity of GABA- and glutamate-containing terminals in the mouse thalamic ventrobasal complex deprived of vibrissal afferents: an immunogold-electron microscopic study.

GABA and glutamate immunogold staining demonstrated that nerve cells of the thalamic ventrobasal complex (VB) of mice were positive exclusively for glutamate. None of the neuronal perikarya reacted the GABA antibody. By using alternate thin sections of the normal VB, it was also shown that large "specific" somatosensory and small corticothalamic terminals, both of which contained spherical synaptic vesicles, exhibited only glutamate-like immunoreactivity. A third axonal type, containing flat-ovoid synaptic vesicles, stained only for GABA. Seventy-five days after coagulation of the vibrissal follicles in newborn mice, a characteristic multiplication of GABA positive axon terminals was observed. In addition, it was demonstrated that, similarly to modified cortical endings (Hámori et al., J. Comp. Neurol. 254:166-183, '86), many GABA positive terminals appeared as specific afferent endings, replacing the missing "specific" vibrissal afferents. This finding shows a remarkable plasticity of inhibitory GABA axons during developmental synaptogenesis and provides further evidence that the size, location, and the type of attachment of presynaptic terminals are dependent on their postsynaptic target.

Morphological alterations in subcortical vibrissal relays following vibrissal follicle destruction at birth in the mouse.

Morphological modifications of two subcortical vibrissal relays were analyzed, following destruction of vibrissal follicles in newborn mice. The volume of the nucleus interpolaris (NI) of the trigeminal nuclear complex in the brainstem decreased by 33%, while the number of its neuronal perikarya decreased only moderately. Vibrissal deafferentation caused no shrinkage of the ventrobasal complex (VB). In the damaged medial vibrissal part of VB (VBm), however, neuronal density was higher than normal, indicating the prevention or retardation of physiologically programmed cell death in the afferentation deprived thalamic somatosensory relay station. It is suggested that the difference in neuron density produced by deafferentation is related to the states of maturation at birth of the two subcortical vibrissal relays. Following vibrissal deafferentation the basic organization of the synaptic neuropil appeared to be similar to the control. Quantitative electron microscopic (EM) analysis revealed, however, an increased number of axon terminals with ovoid synaptic vesicles in both deafferented relay stations. The increased density of gamma-aminobutyric acid (GABA)-immunostained boutons observed in the VBm following vibrissal deprivation suggested a compensatory increase most probably of the inhibitory axon endings. Quantitative EM analysis also provided evidence that many or most of the specific afferent terminals in the damaged VBm were not identical with but were substitutes for the original "vibrissal" specific afferents. Forty percent of all "specific" afferents were shown to be modified corticothalamic terminals. The modification and the resemblence of some cortical endings to specific afferents demonstrated the morphogenetic plasticity of synaptogenesis in these terminals during development as well as the importance and inductive potential of the postsynaptic target in the differentiation of presynaptic axon terminals.

[Organization of the nervous system after coagulation of the follicles of mystacial vibrissae in the newborn mouse: an example of neuronal plasticity]. / L'organisation du système nerveux après coagulation des follicules des vibrisses mystaciales chez la souris nouveau-née: un exemple de plasticité neuronale.

In the mouse the vibrissae and the common fur of the head are a good model of the so called neural plasticity. The characteristics of this model are: the pattern of implantation of the vibrissae at the periphery and that of the arrangement of barrels in the contralateral cortical projection area of vibrissae as well as that of the "barreloïds" in the subcortical vibrissal relays (somato sensory thalamus and trigeminal nuclear complex) are homeomorphic with one another. Each barrel and "barreloïd" receives projections from one vibrissa. Moreover at the level of the cortex these projections are also in register with projections from ipsilateral vibrissae. Head fur hairs project to well defined but entirely distinct areas. Destruction of vibrissae follicles at birth beside preventing barrel and barreloïd formation in the CNS, leads to several morphological changes: degeneration of the primary sensory neurons innervating vibrissae in the trigeminal ganglion, thus degeneration of their central axons and the corresponding terminals in the trigeminal vibrissal relays changes in the distribution of the activity of succinate dehydrogenase in the IVth layer of the cortical vibrissal area and in the corresponding subcortical relays, from the normal discrete (barrel hollow) pattern--corresponding to the clustered vibrissal afferents--to a continuous band, keeping a normal level of activity, excepted in the trigeminal vibrissal relays and a remarkable preservation of cortical thickness but a notable atrophy in the trigeminal vibrissal projection areas. Beside upsetting the anatomy vibrissae follicle destruction causes marked functional changes an outstanding take-over of the deafferented cortical vibrissal area (still identifiable from projections of vibrissae ipsilateral to it) by the head fur hairs this take over exist also in the subcortical vibrissal relays a change in the thalamo-cortical connections. Modifications in the organization of connections are initiated by the loss of the primary sensory neurons innervating vibrissae, in the trigeminal ganglion and results only from early lesions. In mice lesioned when adults the loss of primary sensory neurons is less important and functional take over by the common fur is not observed.

A morphometric study of mouse trigeminal roots after unilateral destruction of vibrissae follicles at birth.

Trigeminal sensory roots were studied in neonatal mice. On the deafferented side, the surface area of the cross-section through the sensory root is diminished by 31% and the number of myelinated fibers is reduced by 21%, but the proportion between myelinated and unmyelinated fibers remains unchanged. The distribution of axonal diameters, analysed in 7 dorso-ventral scanning bands through the sensory roots, indicates a loss or eventually an atrophy of large myelinated axons in the medial two thirds of the sensory root. In both control and deafferented sides the diameter of the myelinated fiber (outside the myelin sheath) is proportional to the axon diameter (inside the myelin sheath). Our results confirm the loss of most of the neurons innervating vibrissae and the lack of regeneration or sprouting in the deafferented root in the newborn mouse.

[Histological changes in the somatosensory thalamus after unilateral coagulation of vibrissa follicles of the muzzle of the newborn mouse]. / Modifications histologiques dans le thalamus somatosensoriel après coagulation unilatérale des follicules des vibrisses du museau chez la Souris nouveaunée.

Light microscopic study of the thalamic ventro-basal complex (VB), after unilateral coagulation of vibrissae follicles in newborn mouse, revealed an excess of neuronal perikarya on the controlateral "deafferented" side as compared to the normal side. The higher density of nerve cells was confined to the vibrissal relay in the medial part of VB nucleus (VBm), whereas the cell number in the non vibrissal-lateral part of this nucleus (VB1) remained on the control level. Electron microscopic investigation of the thalamic vibrissal relay has shown signs of a modified synaptogenesis on the "deafferented" side: (a) the number of specific afferents has diminished and in contrast to the normal side, most of the specific sensory terminals contain small spheroid synaptic vesicles and (b) the number of axon terminals with ovoid pleomorphic vesicles has been doubled.

Reorganization of thalamo-cortical connections in mice dewhiskered since birth.

Localizations of thalamic relay neurons of vibrissae, common fur of the muzzle and head, as well as those projecting to the cortical vibrissal field in mice with vibrissae coagulated at birth, have been studied by retrograde transport of peroxydase. The tracer was injected in the corresponding cortical areas. In coagulated mice, labeled thalamic neurons were situated in the ventro-basal complex anterior to its vibrissa part, corresponding to the area labeled after intracortical injection of the muzzle and head fur area. These results indicate a reorganization in the origin of thalamo-cortical afferents in coagulated mice.

[Localization in the gasserian ganglion of axons innervating the common hairs of the mystacial pad in the normal adult rat and in rats dewhiskered at birth]. / Localisation dans le ganglion de Gasser des axones innervant les poils de fourrure commune du bourrelet mystacial chez le rat adulte normal et chez le rat privé de vibrisses à la naissance.

The neurons which innervate the small common hairs of the mystacial pad are shown to be located in the dorsomedial part of the ganglion of Gasser. In ganglia atrophied as a consequence of early destruction of vibrissae follicles, neurons that innervate these small hairs are still active.

A morphometric study of mouse trigeminal ganglion after unilateral destruction of vibrissae follicles at birth.

A morphometric study of the trigeminal ganglion after unilateral vibrissae follicles' coagulation in newborn mice has shown the following: (a) a 42.8% decrease of the total volume of the ganglion on the deafferented side with reference to the normal side; a 61.5% decrease of the ophthalmic-maxillary part of the ganglion where neurons whose axons innervate vibrissae follicles are located, and only a 24.1% decrease in the common part; (b) a 54.8% decrease of the neuronal cell body volume in the ophthalmic-maxillary part and practically no change in the common part, and (c) a 64.5% decrease of the volume occupied by the nerve fibers in the ophthalmic-maxillary part and only a 28.1% decrease in the common part. A comparison of the section areas in ganglion and of the bulk area of neuronal cell bodies at different levels has also been performed. Counting of the neuronal cell bodies in the ophthalmic-maxillary part of the ganglion indicated a mean neuronal loss of 36.5%. Peripheral reinnervation of the common fur by regenerated axons of neurons which previously innervated vibrissae, although unlikely, cannot be completely excluded.

Cortical organization of the postero-medial barrel-subfield in mice and its reorganization after destruction of vibrissal follicles after birth.

The postero-medial barrel-subfield (PMBSF) of the SI cortex of normal adult mice contains clusters of cells called "barrels". Each barrel histochemically shows increased activity of succinate, lactate, and glucose-6-phosphate dehydrogenase and also GABA-T activity. Some neuronal perikarya in the barrel walls show GABA-T activity. Mitochondrial alpha-GPDH and AChE show equal activities in the hollows and in the walls of the barrels. On this cortical vibrissa field, the contralateral and ipsilateral vibrissae project somatotopically in a way which coincides with the barrels. The mystacial vibrissae and the common fur of the muzzle project to different loci. The cortical surface area for the normal fur is 0.025 mm2, whereas the cortical vibrissal area is 1.0 mm2. In mice with lesioned whisker pads the succinate-dehydrogenase activity of the IVth layer in the vibrissal area becomes a continuous sheet similar to the adjacent IVth layer, the thickness of the cortex is relatively preserved, and the total enzyme activities, biochemically assayed, are unchanged. These features can be explained by a functional substitution. In mice with whisker pads lesioned since birth, the vibrissal area can still be identified by the projections from ipsilateral vibrissae (undamaged side). This vibrissal area, and this alone, is found to be invaded by projections from the contralateral common fur of the muzzle. Experimental data suggest that the compensatory process may result from an invasion of the vibrissal area by a new set of ascending fibers, and not merely from axonal sprouting either at the periphery or at the cortical level.

Projections on the cortical somatic I barrel subfield from ipsilateral vibrissae in adult rodents.

In adult rats and mice, ipsilateral projections to SI posteromedial barrel subfield (PMBSF) are demonstrated for mystacial vibrissae (sinus hairs). Mechanical stimulation with angular deflections in the 2-5 degrees range, elicits potentials in limited areas of SI whose geometric centers coincide for two homologous (contra- and ipsilateral) vibrissae. The cortical domains for two adjacent vibrissae overlap one another slightly. Phase reversal of potentials and unit discharges are also present within the cortex. Ablation of the SI area contralateral to the SI area under study completely abolishes the ipsilaterally projected potentials. It is proposed that ipsilateral responses are mediated via the corpus callosum with an extra delay of 4-5 msec, thus giving each hemisphere the opportunity to compare vibrissal information originating from the two mystacial pads.

Projections of the common fur of the muzzle upon the cortical area for mystacial vibrissae in rats dewhiskered since birth.

In normal adult rats, the mystacial vibrissae and the common fur of the snout project at different loci on the SI cortex. The surface area of the normal fur projection is 0.8 mm2, whereas the vibrissa field amounts to 3-4 mm2. In rats dewhiskered since birth, the vibrissa area can still be identified through the projections from ipsilateral vibrissae (undamaged side). It is shown that in the absence of the vibrissae since birth, the vibrissa area, and this alone, is invaded by projections from the contralateral fur (damaged side).

Postnatal ontogenesis of potentials elicited in the barrelfield of mice by stimulation of the maxillary nerve.

Evoked potentials (laminar analysis and latencies) and unit discharges upon electrical stimulation of the maxillary branch of the trigeminal nerve are studied in mice between postnatal days (PN) 8 and 20. Evoked potentials are negative at the surface of the cortex until PN 16. Latencies reach adult values by the end of the third postnatal week. Comparison with rats shows that mice are relatively less mature than rats at same postnatal ages. A comparison of electrophysiological events and anatomical data shows that between PN 8 and 10 electrical activity is limited to the marginal layer and the outer part of the cortical plate. Layer IV, the layer than contains the barrels, becomes active after PN 12. The subplate layer is found active after PN 16.

[Comparative development of the mammalian nervous system (author's transl)]. / Ontogenèse comparée du système nerveux des mammifères.

By collecting the results of research from different laboratories it has been possible to picture the probable sequence in which the nervous system develops in certain mammalian species. As the present report is to be referred to current conceptions of the development of the nervous system, special attention will be pain to comparative aspects of the question. Mammalian forms vary greatly in degree of maturity at birth, ranging from the fetus-like newborn rat to the highly mobile, almost self-sufficient, guinea-pig. As identical sequences of development will be demonstrated in both categories of mammals attention will be devoted to discussing the criteria which condition our trusting this sequence of development. Lastly, Man will be considered. It is not easy to decide whether man is a true altricial species or in what sense he can be considered as a special case of precocial species. This point is discussed: Man is altricial from the motor point of view. He is precocial from the sensory point of view and sleep develops during embryonic life in this species.

[Functional maturation of the somatosensory neocortex S1 in the rat. Electrophysiological and histochemical study (author's transl)]. / Maturation fonctionnelle du néocortex somatosensoriel S1 chez le rat: étude électrophysiologique et histoenzymologique.

The functional maturation of the somatosensory neocortex has been studied using the projection areas of the whiskers. Natural stimulation of the whiskers evokes global potentials and unitary responses from the 4th postnatal day on. From the 2nd postnatal week the characteristics of the unit responses approximate in latency, topographic organisation of the projections, coding of the directions and temporal characteristics of the stimulation those of the adult. The histochemical activity of succinyl dehydrogenase is demonstrated in layer IV a little before the first electrophysiological response but the typical massed organisation is only seen from the 5th postnatal day. During maturation optical densitometry shows a rapid rise in enzyme activity untill the 7th postnatal day then a slower rise up to the 21st day after which it stabilises.