Environmental enrichment influences neuronal stem cells in the adult crayfish brain

Abstract

New neurons are incorporated throughout life into the brains of many vertebrate and non-vertebrate species. This process of adult neurogenesis is regulated by a variety of external and endogenous factors, including environmental enrichment, which increases the production of neurons in juvenile mice and crayfish. The primary goal of the present study was to exploit the spatial separation of the neuronal precursor cell lineage in crayfish to determine which generation(s) of precursors is altered by environmental conditions. Further, in crayfish, an intimate relationship between the 1st generation neuronal precursors (stem cells) and cells circulating in the hemolymph has been proposed (Zhang et al., 2009). Therefore, a second goal was to assess whether environmental enrichment alters the numbers or types of cells circulating in the hemolymph. We find that neurogenesis in the brains of sexually differentiated procambarid crayfish is enhanced by environmental enrichment as previously demonstrated by Sandeman and Sandeman (2000) in young, sexually undifferentiated Cherax destructor. We also show that environmental enrichment increases the cell cycle rate of neuronal stem cells. While there was no effect of environment on the overall numbers of cells circulating in the hemolymph, enrichment resulted in increased expression of glutamine synthetase, a marker of the neuronal stem cells, in a small percentage of circulating cells; there was little or no expression of this enzyme in hemolymph cells extracted from deprived animals. Thus, environmental enrichment influences the rate of neuronal stem cell division in adult crayfish, as well as the composition of cells circulating in the hemolymph.

Adult Neurogenesis: Ultrastructure of a Neurogenic Niche and Neurovascular Relationships

“…In our experiments in P. clarkii , a large cell in an “invariant position” has never been observed in adult niches [4] , [5] , [6] , [54] , [55] or associated with the protoniche as it emerges [24] . Further, the relatively slow cycling of the cells that constitute the emerging protoniche [24] and the adult niche [6] is in contrast to the rapid cycling of neuroblasts.…”

Adult Neurogenesis: Ultrastructure of a Neurogenic Niche and Neurovascular Relationships

“…In our experiments in P. clarkii , a large cell in an “invariant position” has never been observed in adult niches [4] , [5] , [6] , [54] , [55] or associated with the protoniche as it emerges [24] . Further, the relatively slow cycling of the cells that constitute the emerging protoniche [24] and the adult niche [6] is in contrast to the rapid cycling of neuroblasts.…”

Enriched Environment Increases PCNA and PARP1 Levels in Octopus vulgaris Central Nervous System: First Evidence of Adult Neurogenesis in Lophotrochozoa

“…In insects and mammals, both the environment and the experience‐based learning affect the adult neurogenesis in term of circuitry reorganization. In insects mushroom bodies, neuroblasts proliferation results an increase in specimens reared in enriched environment compared to specimens housed in sensory deprivation, also demonstrated in analogue experiments on crustaceans (Hansen and Schmidt, , ; Sullivan et al., ; Ayub et al., ), and the ablation of neuroblasts implies a damage of learning capabilities (Scotto‐Lomassese et al., , , ; Cayre et al., ). In mammals, both enriched environment and cognitive stimulation influence proliferation and survival of newborn interneurons (Rochefort et al., ; Shors et al., ; Clemenson et al., ), and their capacity to form new synapses (Kondo et al., ; Kumazawa‐Manita et al., ; Lepousez et al., ), in olfactory bulb as well as in hippocampus, as shown in numerous behavioral experiments (Kempermann and Gage, ; Magavi et al., ; Snyder et al., ; Lepousez et al., ).…”

Neurogenesis in the central olfactory pathway of adult decapod crustaceans: development of the neurogenic niche in the brains of procambarid crayfish

“…The origins of cell clusters 9 and 10 and the migratory streams have been identified, but the cellular origins of the protoniche cells remain obscure. These findings contribute to our understanding of neurogenesis in the juvenile and adult stages of the closely related crayfish P. clarkii [ 13 , 14 , 16 , 25 , 27 , 28 , 30 , 31 , 46 , 47 ].…”

Adult Neurogenesis: Ultrastructure of a Neurogenic Niche and Neurovascular Relationships

“…In our experiments in P. clarkii , a large cell in an “invariant position” has never been observed in adult niches [4] , [5] , [6] , [54] , [55] or associated with the protoniche as it emerges [24] . Further, the relatively slow cycling of the cells that constitute the emerging protoniche [24] and the adult niche [6] is in contrast to the rapid cycling of neuroblasts.…”

Enriched Environment Increases PCNA and PARP1 Levels in Octopus vulgaris Central Nervous System: First Evidence of Adult Neurogenesis in Lophotrochozoa

“…In insects and mammals, both the environment and the experience‐based learning affect the adult neurogenesis in term of circuitry reorganization. In insects mushroom bodies, neuroblasts proliferation results an increase in specimens reared in enriched environment compared to specimens housed in sensory deprivation, also demonstrated in analogue experiments on crustaceans (Hansen and Schmidt, , ; Sullivan et al., ; Ayub et al., ), and the ablation of neuroblasts implies a damage of learning capabilities (Scotto‐Lomassese et al., , , ; Cayre et al., ). In mammals, both enriched environment and cognitive stimulation influence proliferation and survival of newborn interneurons (Rochefort et al., ; Shors et al., ; Clemenson et al., ), and their capacity to form new synapses (Kondo et al., ; Kumazawa‐Manita et al., ; Lepousez et al., ), in olfactory bulb as well as in hippocampus, as shown in numerous behavioral experiments (Kempermann and Gage, ; Magavi et al., ; Snyder et al., ; Lepousez et al., ).…”

Neurogenesis in the central olfactory pathway of adult decapod crustaceans: development of the neurogenic niche in the brains of procambarid crayfish

“…The origins of cell clusters 9 and 10 and the migratory streams have been identified, but the cellular origins of the protoniche cells remain obscure. These findings contribute to our understanding of neurogenesis in the juvenile and adult stages of the closely related crayfish P. clarkii [ 13 , 14 , 16 , 25 , 27 , 28 , 30 , 31 , 46 , 47 ].…”

Adult Neurogenesis: Ultrastructure of a Neurogenic Niche and Neurovascular Relationships

“…In our experiments in P. clarkii , a large cell in an “invariant position” has never been observed in adult niches [4] , [5] , [6] , [54] , [55] or associated with the protoniche as it emerges [24] . Further, the relatively slow cycling of the cells that constitute the emerging protoniche [24] and the adult niche [6] is in contrast to the rapid cycling of neuroblasts.…”

Enriched Environment Increases PCNA and PARP1 Levels in Octopus vulgaris Central Nervous System: First Evidence of Adult Neurogenesis in Lophotrochozoa

“…In insects and mammals, both the environment and the experience‐based learning affect the adult neurogenesis in term of circuitry reorganization. In insects mushroom bodies, neuroblasts proliferation results an increase in specimens reared in enriched environment compared to specimens housed in sensory deprivation, also demonstrated in analogue experiments on crustaceans (Hansen and Schmidt, , ; Sullivan et al., ; Ayub et al., ), and the ablation of neuroblasts implies a damage of learning capabilities (Scotto‐Lomassese et al., , , ; Cayre et al., ). In mammals, both enriched environment and cognitive stimulation influence proliferation and survival of newborn interneurons (Rochefort et al., ; Shors et al., ; Clemenson et al., ), and their capacity to form new synapses (Kondo et al., ; Kumazawa‐Manita et al., ; Lepousez et al., ), in olfactory bulb as well as in hippocampus, as shown in numerous behavioral experiments (Kempermann and Gage, ; Magavi et al., ; Snyder et al., ; Lepousez et al., ).…”

Neurogenesis in the central olfactory pathway of adult decapod crustaceans: development of the neurogenic niche in the brains of procambarid crayfish

“…The origins of cell clusters 9 and 10 and the migratory streams have been identified, but the cellular origins of the protoniche cells remain obscure. These findings contribute to our understanding of neurogenesis in the juvenile and adult stages of the closely related crayfish P. clarkii [ 13 , 14 , 16 , 25 , 27 , 28 , 30 , 31 , 46 , 47 ].…”