The effect of impulse blockage on cytochrome oxidase activity in the cat visual system

doi:10.1016/0006-8993(83)90622-4

Brain Research

Volume 261, Issue 2, 21 February 1983, Pages 185-193

https://doi.org/10.1016/0006-8993(83)90622-4 Get rights and content

Abstract

Our previous studies have indicated that sensory deprivation in the developing and mature nervous system could bring about an adjustment in oxidative metabolism of neurons demonstrable by cytochrome oxidase (C.O.) histochemistry^45,46,49. Since sensory deprivation potentially involves changes in several parameters, such as natural stimuli, action potentials and axoplasmic transport, we wished to know if the cessation of primary afferent impulses could produce enzymatic adjustment in the postsynaptic neurons. Tetrodotoxin (TTX), in a dosage determined by Stryker (personal communication) to block action potentials without blocking axoplasmic transport, was injected intravitreally into one eye of 10 adult cats every 3 days for total periods of 1, 2, 4, 5.5 or 6 weeks respectively. After perfusion, the brains were processed for C.O. histochemistry. The results indicated that: (1) a decreased level of C.O. activity was observed in the lateral geniculate (LGN) laminae innervated by the injected eye as well as in area 17 of all animals; (2) changes were discernible after 1 week, which was the earliest time examined, but became progressively more prominent up to 6 weeks; (3) within the LGN, the ipsilateral lamina A₁ consistently appeared more severely affected than the contralateral lamina A; (4) the monocular segment of the affected lamina A exhibited a high level of enzyme activity, indicating that its oxidative metabolism might be sustained by other factor(s) or synaptic activity; (5) within the binocular representation of the striate cortex, a banding pattern of high and low C.O. activity in lamina IV became progressively more prominent with longer survivals. In cats subjected to 4 weeks of TTX treatment and 6 weeks of recovery, the enzymatic levels in the affected LGN and cortical laminae were comparable to that of the normal. This indicated that the dosage used apparently did not damage the neural pathways. Thus, impulse blockage can cause a decrease in the level of cytochrome oxidase activity in the affected postsynaptic neurons, and the maintenance of functional and enzymatic integrity of postsynaptic neurons in the adult is dependent upon viable presynaptic impulse conduction.

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In general, capillary density correlates with three indicators of metabolic activity: 2-deoxyglucose labeling, number of mitochondria, and staining for cytochrome oxidase, a mitochondrial enzyme involved in oxidative metabolism. For example, gray matter takes up more 2-deoxyglucose [49], stains more heavily for cytochrome oxidase [103], and is better supplied with blood vessels than white matter [15,23]. In somatosensory cortex, the barrels representing individual vibrissae stain more heavily for cytochrome oxidase [104] and contain more capillaries than surrounding cortex [74,78].
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Neurotransmitters are prominent candidates for trans-cellular signals that influence the development of the CNS. The present study has examined the effect of glutamate on survival, differentiation and metabolic activity of cultured rat retinal ganglion cells at 3 days in vitro. Retinal cultures from neonatal Wistar rats were treated with glutamate for 48 h. The metabolic activity was markedly increased in the retinal ganglion cells exposed to 20 μM glutamate. This was accompanied by an enhanced survival of these neurons. The number of differentiated retinal ganglion cells as determined by microtubule-associated protein-2 labeling was significantly increased following exposure to low but not higher doses of glutamate. The effect of glutamate on the metabolic activity and differentiation was blocked by tetrodotoxin.
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Extrinsic modulation of tonic nerve activity has proven to be a useful strategy for locating brain regions in both mammalian and nonmammalian sensory systems. Since tonic reactivity of cytochrome oxidase (COX) depends upon tonic neuronal activity, loss of constant input results in a down-regulation of COX and a concomitant loss of its histochemical reactivity [22,46–51]. This loss of tonic activity may be reflected as a decrease in the intensity of COX reactivity through at least two to three serial synapses away from the site of intervention.
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The effect of impulse blockage on cytochrome oxidase activity in the cat visual system

Abstract

Neurosci. Lett.

Brain Research

Exp. Neurol.

Brain Research

Brain Research

Brain Research

Trends in Neurosci.

Exp. Neurol.

Brain Research

Brain Research

Brain Research

Motor neuron sprouting induced by prolonged tetrodotoxin block of nerve action potentials

Nature (Lond.)

The effect of disuse on cholinergic enzymes

J. Physiol. (Lond.)

Quantitative histochemical effects of whisker damage on single identified cortical barrels in the adult mouse

J. Neurosci.

Neurotrophic regulation of two properties of skeletal muscle by impulse-dependent and spontaneous acetylcholine transmission

J. Neurosci.

Effect of midbrain raphe and lateral mesencephalic stimulation on spontaneous and evoked activity in the lateral geniculate of the cat

Exp. Brain Res.

Laminar differences in receptive field properties of cells in cat primary visual cortex

J. Physiol. (Lond.)

Sprouting of optic tract projections in the brainstem of the rat

J. comp. Neurol.

Binocular competition in the control of geniculate cell growth

J. comp. Neurol.

Experiments to determine whether retinogeniculate axons can form translaminar collateral sprouts in the dorsal lateral geniculate nucleus of the cat

J. comp. Neurol.

An analysis of the retinal afferents to the cat's medial interlaminar nucleus and to its rostral thalamic extension, the ‘geniculate wing’

J. comp. Neurol.

The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat

J. comp. Neurol.

Pharmacological modifications of the sodium channels of frog nerve

J. gen. Physiol.

Corticofugal influence on activity of lateral geniculate neurons in the cat

J. Neurophysiol.