Cyclic structural changes of endoplasmic reticulum and Golgi complex in hippocampal neurons of ground squirrels during hibernation

Repetitive remodeling and renewal of the cytoplasmic structures realizing protein synthesis accompanies the cycling of the ground squirrels between torpor and arousal states during hibernation season. Previously, we have shown the partial loss of ribosomes and inactivation of the nucleolus in pyramidal neurons in the hippocampus CA3 area at each bout of torpor with their rapid and full recovery after warming up. In the present paper, we describe reversible structural changes of the endoplasmic reticulum (ER) and Golgi complex (GC) in these neurons. The transformation of the ER form from mainly granular stacks of flattened cisternae to smooth tubules occurs at every entrance in torpor, while the reverse change happens at arousal. The torpor state is also associated with GC fragmentation and loss of their flattened cisternae, i.e., dictiosomes. In neurons, the appearance of the autophagosomal vacuoles containing fragments of membrane structures and ribosomes in torpor state is a sign of the partial destruction of ER and GC. Granular ER restoration, perhaps through assembly from the multilamellar membrane structures, bags or whorls begins in the middle of the torpor bout, while GC dictiosomes reappear only during warming. The ER and GC completely restore their structure 2–3 h after the beginning of arousal. Thus, hibernation represents an example of the structural adaptation of the nerve cell to deep changes in functional and metabolic activity through both the active destruction and renewal of ribosomes, ER, and GC. Perhaps, namely the incomplete ER autophagosomal degradation in torpor provides its rapid renewal at arousal through the reassembly from the preserved fragments.