Experience induces structural and biochemical changes in the adult primate brain

Abstract

Primates exhibit complex social and cognitive behavior in the wild. In the laboratory, however, the expression of their behavior is usually limited. A large body of literature shows that living in an enriched environment alters dendrites and synapses in the brains of adult rodents. To date, no studies have investigated the influence of living in a complex environment on brain structure in adult primates. We assessed dendritic architecture, dendritic spines, and synaptic proteins in adult marmosets housed in either a standard laboratory cage or in one of two differentially complex habitats. A month-long stay in either complex environment enhanced the length and complexity of the dendritic tree and increased dendritic spine density and synaptic protein levels in the hippocampus and prefrontal cortex. No differences were detected between the brains of marmosets living in the two differentially complex environments. Our results show that the structure of the adult primate brain remains highly sensitive even to modest levels of experiential complexity. For adult primates, living in standard laboratory housing may induce reversible dendritic spine and synapse decreases in brain regions important for cognition.

Fig. 1.

Environmental complexity enhances dendritic spine density in the adult marmoset brain. (A) Photograph of a marmoset in a complex environment, representing ≈40% of a complex single cage, with branches, vegetation, and objects typically included in the complex environment: a straw nest, a tree stump with holes, wooden swings, a wooden ladder, and blocks. (B) Photomicrograph of a Golgi impregnated CA1 pyramidal neuron, with close-up views of representative CA1 apical (a-c) and basal (d-f) dendrites, from animals in control (a and d), and complex single (b and e) and complex double cages (c and f). Arrows point to spines. (C) Photomicrograph of a DiI-labeled PFC pyramidal neuron (green color assigned for illustration purposes), with close-up views of a representative basal dendritic segment (Upper Right) and a cortico-striatal axonal segment (Bottom Right). Arrows point to spines and varicosities, respectively. (D) Marmosets living in complex environments for 4 weeks have greater dendritic spine density on several types of Golgi-impregnated neurons in the hippocampus and the PFC, compared with marmosets living in standard laboratory environments. Error bars represent SEM; asterisks reflect statistically significant differences from control group on Tukey post hoc comparison: ^*, P < 0.05; ^**, P < 0.01; ^***, P < 0.001. (E) Marmosets living in complex environments have greater dendritic spine density on DiI-labeled neurons compared with animals living in standard laboratory conditions. (F) No differences in intervaricosity spacing on cortico-striatal axons were observed for marmosets living in standard and two types of complex housing.

Fig. 2.

Environmental complexity enhances synaptic protein levels. (Left) Photomicrographs of hippocampal sections immunostained for spine and synapse-related proteins AMPA receptor subunit GluR2, synaptophysin, and spinophilin. (Right) Optical intensity index for GluR2 (Top), synaptophysin (Middle) and spinophilin (Bottom). Marmosets living in complex housing showed enhanced levels of GluR2 and synaptophysin in the hippocampus and the PFC, and of spinophilin in the hippocampus.