Distribution of the perforant path following selective elimination of granule cells

doi:10.1016/0014-4886(78)90045-6

Experimental Neurology

Volume 62, Issue 1, October 1978, Pages 122-132

https://doi.org/10.1016/0014-4886(78)90045-6 Get rights and content

Abstract

X-irradiation of the developing hippocampus of the rat causes partial elimination of the dentate granule cells and results in an alteration in the afferent topogrophy found in this region. With the loss of their normal targets the axons and terminals of the perforant path, major input to the dentate gyrus, hypertrophy by 50% in regio superior pyramidal cell fields. Commissural and associational inputs to this region are concomitantly reduced. This observation is interpreted to support the hypothesis that afferent topography in the hippocampus is the result of competitive interactions between developing fiber systems.

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Selective working memory impairments following intradentate injection of colchicine: attenuation of the behavioral but not the neuropathological effects by gangliosides GM1 and AGF2
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Bilateral injection of 3.5 μg of colchicine into the dentate gyrus produced specific learning and memory impairments together with a selective pattern of neuropathology. Animals injected with colchicine exhibited a significant impairment in their ability to perform the working memory, but not the reference memory, component of a multiple component T-maze task. These deficits were transient and over time all animals were able to reacquire task to preoperative levels of performance. Histological analyses revealed that intradentate injection of colchicine produced 1) a significant decrease in the width of both the superior and inferior blades of the dentate gyrus reflecting the extensive loss of granule cells, 2) a related decrease in the size of the dentate molecular layer, and 3) a decrease in the number of cholinergic neurons in the medial septum. The second phase of the experiment demonstrated that gangliosides GM1 and AGF2 did not prevent the initial impairments in working memory performance induced by colchicine but rather accelerated the rate at which it recovered. The gangliosides did not decrease the exent of neuronal damage; there was no sparing of granule cells in the dentate gyrus or cholinergic neurons in the medial septum. These data further support a role for the hippocampus in working memory processes and they also indicate that gangliosides GM1 and AGF2 might be useful for treating the behavioral deficits induced by hippocampal damage.
Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields of the rat hippocampal formation
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The distribution of enkephalin immunoreactivity (EI) in the molecular layer of the hippocampal formation corresponded to the terminal field of the lateral perforant path and the lateral temporoammonic tract. The distribution of cholecystokinin immunoreactivity (CI) in the molecular layer of the hippocampal formation corresponded to the established terminal field of the medial temporoammonic tract. The exception was a CI band at the deep part of the molecular layer throughout the regio superior. Accordingly, an additional terminal field of the medial temporoammonic tract is suggested. Selective lesion of the entorhinal afferents to the hippocampus and the area dentata resulted in a disappearance of EI throughout the molecular layer with no affection of CI and vice versa. Neonatally X-ray irradiated hippocampi were examined as they appear in the adult animal. These animals are known to possess an altered relation between the granule cells of area dentata and the perforant path zones extending beyond a reduced medial blade into the stratum oriens of the regio inferior. In such animals EI and CI revealed the same pattern of changes by following the perforant path zones into stratum oriens due to neonatal X-ray irradiation. Accordingly, the perforant path may contain EI and CI independent of the granule cell dendrites. Based on a discussion of these observations we conclude that enkephalin immunoreactivity is localized in terminals of the lateral perforant path and the lateral temporoammonic tract and that cholecystokinin immunoreactivity is localized in the terminals of the medial perforant path and the medial temporoammonic tract.
Adenylate cyclase responses in rat brain after unilateral postnatal X-irradiation
1982, Experimental Neurology
When unilateral x-irradiation was directed to the area of the posterior cerebral cortex overlying the hippocampus of the neonatal rat, histologic damage was observed in the hippocampus (previous observations), pia-arachnoid (cellular proliferation), and retina (two layers of bipolar cells and damage to visual receptor area and diminished number of ganglion cells). Light microscopy did not reveal any remarkable cellular alterations in parenchymal or capillary tissue of the posterior cerebrum. The most prominent deficits in norepinephrine sensitivity of adenylate cyclase occurred in the pia-arachnoid > hippocampus > posterior cerebrum. The associated capillaries were unchanged and in the retina the enzyme displayed an enhanced sensitivity to dopamine.
Axo-somatic synapses in the normal and X-irradiated dendate gyrus: Factors affecting the density of afferent innervation
1982, Brain Research
The density of synaptic input to the somata of dentate gyrus granule cells was examined utilizing quantitative electron microscopic techniques. In control (non-irradiated) material, greater numbers of axo-somatic synapses were observed in the superficial, earlier-generated cells as compared to the deep, later-generated cells. We further studied the X-irradiated dendate gyrus, in which the majority of granule cells were destroyed during postnatal genesis. The surviving cells displayed a density of innervation on their somata which exceeded that observed in either layer of the control material. These data are discussed in terms of the possible contribution of afferent-target cell interactions to the regulation of the density of synaptic innervation.
The development of the cholinergic system in rat hippocampus following postnatal X-irradiation
1981, Brain Research
Postanatal X-irradiation of the rat hippocampus results in a marked reduction in the number of the postnatally developing granular neurons in the dentate gyrus and also caused a marked increase in the specific activity of acetylcholinesterase (AChE) and choline acetyltransferase (CAT) and a slight but consistent increase in the activity per whole hippocampus of AChE. The effect of irradiation on the granular neurons and on the cholinergic enzymes was found to be dose and age dependent. Drastic increase in specific enzymatic activities is also observed in the irradiated cerebellum whose granular neurons differentiate postnatally and to a lesser extent in the cerebral cortex in which cell formation is accomplished prior to birth.
Staining for AChE activity revealed enhanced staining in the molecular layer and the hilar zone of the irradiated dentate gyrus, and in the striatum lucidum of area CA3 which corresponds to the projection area of the mossy fibers. Enhanced staining in area CA1 and subiculum was noticed especially in the supra- and infrapyramidal layers. Biochemical analysis demonstrated that AChE and CAT activities were 140–180% higher in the subareas of the irradiated vs non-irradiated hippocampus.
The development and distribution of the postsynaptic muscarinic receptors in the irradiated hippocampus by [³H]quinuclidinyl benzilate (QNB)-binding were also studied. It was found that the elimination of the postnatally formed neurons does not appear to change the developmental pattern of the [³H]QNB-binding sites but reduced receptor level to about 75% of control to adulthood. Measuremnts of the [³H]QNB-binding in the subareas within the hippocampus revealed marked reduction in the specific [³H]QNB-binding in the molecular layer of the dentate gyrus but not in other subareas. However, the reduction in [³H]QNB-binding sites in the dentate is not as drastic as the reduction in the number of granular neurons. It is suggested that muscarinic sites may be located on early formed neurons, non-cholinergic afferents, or glial elements in this area.

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²: Drs. Gerbrandt and Wheeler are at California State University at Northridge and Drs. Rose and Lynch are at U.C. Irvine.

¹: Supported by Grants MH 19792-05 from MIMH and BMS 7202237-3 from NSF and a Research Career Development Award to G. L.

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Distribution of the perforant path following selective elimination of granule cells

Abstract

Brain Res.

Brain Res.

Brain Res.

Behavioral effects of interference with the postnatal acquisition of hippocampal granule cells

Nature New Biol.

Radiation-induced interference with postnatal hippocampal cytogenesis in rats and its long-term effects on the acquisition of neurons and glia

J. Comp. Neurol.

Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system

Brain Res.