Timing of neurodegeneration and beta‐amyloid (Aβ) peptide deposition in the brain of aging kokanee salmon

Abstract

Brains of kokanee salmon (Oncorhynchus nerka kennerlyi) in one of four reproductive stages (sexually immature, maturing, sexually mature, and spawning) were stained with cresyl violet and silver stain to visualize neurodegeneration. These reproductive stages correlate with increasing somatic aging of kokanee salmon, which die after spawning. Twenty-four regions of each brain were examined. Brains of sexually immature fish exhibited low levels of neurodegeneration, whereas neurodegeneration was more marked in maturing fish and greatest in spawning fish. Neurodegeneration was present in specific regions of the telencephalon, diencephalon, mesencephalon, and rhombencephalon. Pyknotic neurons were observed in all regions previously reported to be immunopositive for A beta. Regions that did not exhibit neurodegeneration during aging included the magnocellular vestibular nucleus, the nucleus lateralis tuberis of the hypothalamus, and Purkinje cells of the cerebellum, all of which also lack A beta; perhaps these regions are neuroprotected. In 14 of 16 brain areas for which data were available on both the increase in A beta deposition and pyknosis, neurodegeneration preceded or appeared more or less simultaneously with A beta production, whereas in only two regions did A beta deposition precede neurodegeneration. This information supports the hypothesis that A beta deposition is a downstream product of neurodegeneration in most brain regions. Other conclusions are that the degree of neurodegeneration varies among brain regions, neurodegeneration begins in maturing fish and peaks in spawning fish, the timing of neurodegeneration varies among brain regions, and some regions do not exhibit accelerated neurodegeneration during aging.

Insights into Biomedicine from Animal Adaptations

“…The initial increase in neuronal pyknosis occurred prior to the deposition of BA in 50% of brain regions and at the same reproductive stage in about 38% (of brain regions). The data of Maldonado et al (68) are consistent with the notion that BA deposition is not the cause of neurodegeneration but perhaps part of a repair process.…”

“…For example, the olfactory system is used by the salmon to return to its natal stream and this function is clearly preserved despite extensive deposits of APP and BA. In a subsequent study, Maldonado et al (68) examined the brains of kokanee salmon prior to spawning for evidence of neuronal degeneration and then characterized the timing of this neurodegeneration with respect to the timing of BA deposition. Twenty fishes were assigned to one of four reproductive stages varying from sexually immature to spawning.…”

A Paradox of Parasite Prolonging the Life of Its Host. Pearl Mussel Can Disable the Accelerated Senescence Program in Salmon

“…Pacific salmon (Salmonidae) inevitably dies after the first spawning as a result of triggering the genetic program of death (Robertson et al ., 1961;Maldonado et al ., 2002).…”

“…Accelerated senescence of Pacific salmon can be prevented by gonadectomy or adrenalectomy. Such operation doubles the lifespan of king salmon from 4 to 8 years (Robertson et al ., 1961;Maldonado et al ., 2002). The biological significance of parental suicide is to provide food for river invertebrates, which are consequently consumed by salmon fry (Ziuganov et al ., 1998).…”

Intraneuronal amyloid precursor protein (APP) and appearance of extracellular β‐amyloid peptide (aβ) in the brain of aging kokanee salmon

“…Increased APP, then, might be produced as a neuroprotective agent (Whitson et al, 1989;Roberts et al, 1991;Kawarabayashi et al, 1991). These two brain regions do not exhibit an increase in neurodegeneration during kokanee brain aging (Maldonado et al, 2002).…”