Growth alteration in the auditory cortex of visually deprived mice

589

456

The oligodendrocyte is the myelin-forming cell in the central nervous system. Despite the close interaction between axons and oligodendrocytes, there is little evidence that neurons influence myelinogenesis. On the contrary, newly differentiated oligodendrocytes, which mature in culture in the total absence of neurons, synthesize the myelinspecific constituents of oligodendrocytes differentiated in vivo and even form myelin-like figures. Neuronal To determine whether the onset of myelination was the consequence only of oligodendrocyte maturation or depended on an axonal signal, we investigated the influence of axonal electrical activity on myelinogenesis. Indeed, action potentials have been demonstrated to play a key role during CNS development, particularly in the visual system (20,21). Here we show that inhibition of electrical activity with the specific Na+ channel blocker tetrodotoxin (TTX) prevents the initiation of myelinogenesis in a system of in vitro myelination using dissociated cultures from embryonic brain and in vivo, in the optic nerve. In addition, with K+ that blocks action potentials by maintaining the cells in a depolarized state, or a-scorpion toxin (a-ScTX), which induces repetitive electrical activity by slowing Na+ channel inactivation, we provide evidence that it is the action potential itself which is responsible for the onset of myelination.

Section: Discussionsupporting

confidence: 91%

Induction of myelination in the central nervous system by electrical activity.

Demerens

Stankoff

Logak

et al. 1996

589

456

“…In support of this interpretation, the cell body size of neurons in whisker pad barrels is enlarged after bilateral enucleation in mice (9). Moreover, in the auditory cortex, the size of pyramidal neurons and the density of spines on their apical dendrites increase following enucleation (21,22). These effects of enucleation on neurons in S1 and Al are consistent with the hypothesis that neural activity promotes growth.…”

Section: Discussionsupporting

confidence: 73%

Effects of increased neural activity on brain growth.

Zheng

Purves²

1995

We have measured the effects of regionally increased metabolic activity-and by inference electrical activity-on cortical growth in the developing rat brain. Cortical growth is significantly and specifically greater in regions of chronically increased activity. This effect of activity on cortical growth may help explain the permanent storage of early experience in the developing nervous system.The mammalian brain grows progressively in postnatal life, increasing in weight about 4-fold from birth to maturity in man and mouse (1-3). In the work reported here we have tested the hypothesis that this gradual enlargement is modulated by experience, regional growth being increased by locally augmented neural activity (4-6).Using the somatosensory cortex of the rat, we have taken advantage of previous studies that showed that the growth of one sensory system in the rodent brain can be enhanced by depriving the animal of a different sensory modality (7-9). Thus, neonatal eye removal in mice causes an enlargement of the cortical barrels (and neurons) that represent the mystacial vibrissae. These studies did not, however, examine levels of neural activity in the affected cortex or relate neural activity to cortical growth. Accordingly, we have asked whether metabolic activity, measured by the index of blood vessel density (4, 10, 11), is increased in the somatic sensory cortex of the enucleated animals and if changes in activity are associated with regionally specific enhancement of cortical growth during development. Since most of the energy demand on neurons is generated by synaptic signaling, local levels of metabolism reflect regional differences in the brain's electrical activity (12-15).Our results show that bilateral eye removal at birth increased capillary density in the primary somatic sensory cortex (S1) and its component parts. Moreover, each of the cortical areas with chronically augmented levels of metabolic activity grew larger than its counterpart in control animals, whereas adjacent cortical areas with normal levels of activity did not. MATERIALS AND METHODSSix litters of male Long Evans (pigmented) rats from Charles River Laboratories were used in these experiments. Half of the pups in each litter underwent bilateral enucleation within 24 hr of birth; the other half served as controls. After inducing surgical anesthesia by cooling (16), both globes were removed. The remaining (control) animals in the litter were anesthetized only. Each litter was kept together until weaning; subsequently, experimental and control animals were fostered three or four per cage until 10-12 weeks of age. The animals were then anesthetized with pentobarbital (250 mg/kg) and perfused as described (4). Serial tangential sections (35 gm) were prepared for cytochrome oxidase histochemistry to demonstrate the primary somatic sensory cortex, the primary auditory cortex, the primary visual cortex, and the striatum. All slides were coded so that measurements were made without knowledge of an animal's history. Images of the ink-fi...

“…It appears, therefore, that somatosensory cortex may be enlarged at the expense of other cortical areas. Atrophy of the visual cortex has indeed been demonstrated after early binocular enucleation in monkeys (15)(16)(17) and after dark-rearing in mice (18). In the latter case, a concomitant hypertrophy of auditory cortex has also been reported.…”

Section: Discussionmentioning

confidence: 88%

Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals.

Rauschecker

Tian

Körte

et al. 1992

128

Cats deprived of vision from birth adapt remarkably well to their situation and show little behavioral impairment. They seem to compensate for their lack of vision by relying more on their auditory and tactile senses. We report here that the facial vibrissae, which are most important for tactile orientation in many animals, show supernormal growth in both cats and mice that have been deprived of vision from birth. Furthermore, the whisker representation in the somatosensory cortical barrel field shows a concomitant enlargement in binocularly enucleated mice: individual barrels are expanded in size by up to one-third. The increased use of the vibrissae in visually deprived animals may stimulate both their own growth and, via activation of the respective neural pathways, the expansion of their central representation.Kittens are born with their eyes closed. When normal eye opening is prevented surgically by means of lid suture, the lids grow together permanently, which precludes all pattern vision (1). Despite their lack of vision, these cats learn to move around with little impairment and show such a high degree of behavioral normality that uninformed observers would hardly guess they could not see (1, 2). Similar compensatory plasticity has been described in young monkeys with early vision impairment (3).There is evidence that visually deprived cats have improved auditory capacities (4,5) and that they make very efficient use oftheir vibrissae (6-8). From casual observation it also appeared to us that the vibrissae were on average longer in lid-sutured cats than in normal cats. We therefore decided to determine whisker lengths and diameters quantitatively in both groups of animals.To reduce the variance of data between animals within each group, it would be advantageous to study animals from the same litter. The small litter size in cats, however, makes this practically impossible. We decided, therefore, to study the effects of visual deprivation also on the vibrissae system in the mouse, which not only has larger litters and less genetic variability but in addition has a distinct anatomical representation of its whiskers in the central somatosensory system, the barrel field (9). We hoped that this might allow us to test for a central change in the vibrissa/barrel system possibly related to somatosensory compensation. MATERIALS AND METHODSVibrissae Measurements in Cats. Whisker lengths were measured in 13 cats that had been deprived of vision by means of binocular lid suture until at least 6 months of age, and in 19 normal control animals of comparable age and weight. In addition, whisker diameter at the base was measured in 12 cats, 6 chosen randomly from each of these groups. Lid sutures had been performed by a standard procedure (1) at the Max-Planck-Institut in Tubingen, Germany, around the time of eye opening, under ketamine/ xylazine anesthesia (25 mg/kg).Whisker lengths were determined in situ, while the cats were anesthetized with ketamine and xylazine. Each vibrissa was stretched with a forceps a...