Brain infusion of α-synuclein oligomers induces motor and non-motor Parkinson's disease-like symptoms in mice

Behav Brain Res. 2017 Aug 30:333:150-160. doi: 10.1016/j.bbr.2017.06.047. Epub 2017 Jun 29.

Abstract

Parkinson's disease (PD) is characterized by motor dysfunction, which is preceded by a number of non-motor symptoms including olfactory deficits. Aggregation of α-synuclein (α-syn) gives rise to Lewy bodies in dopaminergic neurons and is thought to play a central role in PD pathology. However, whether amyloid fibrils or soluble oligomers of α-syn are the main neurotoxic species in PD remains controversial. Here, we performed a single intracerebroventricular (i.c.v.) infusion of α-syn oligomers (α-SYOs) in mice and evaluated motor and non-motor symptoms. Familiar bedding and vanillin essence discrimination tasks showed that α-SYOs impaired olfactory performance of mice, and decreased TH and dopamine levels in the olfactory bulb early after infusion. The olfactory deficit persisted until 45days post-infusion (dpi). α- SYO-infused mice behaved normally in the object recognition and forced swim tests, but showed increased anxiety-like behavior in the open field and elevated plus maze tests 20 dpi. Finally, administration of α-SYOs induced late motor impairment in the pole test and rotarod paradigms, along with reduced TH and dopamine content in the caudate putamen, 45 dpi. Reduced number of TH-positive cells was also seen in the substantia nigra of α-SYO-injected mice compared to control. In conclusion, i.c.v. infusion of α-SYOs recapitulated some of PD-associated non-motor symptoms, such as increased anxiety and olfactory dysfunction, but failed to recapitulate memory impairment and depressive-like behavior typical of the disease. Moreover, α-SYOs i.c.v. administration induced motor deficits and loss of TH and dopamine levels, key features of PD. Results point to α-syn oligomers as the proximal neurotoxins responsible for early non-motor and motor deficits in PD and suggest that the i.c.v. infusion model characterized here may comprise a useful tool for identification of PD novel therapeutic targets and drug screening.

Keywords: Anxiety-like behavior; Dopamine; Intracerebroventricular (i.c.v.) infusion; Olfactory bulb; Olfactory dysfunction; Parkinson’s disease; Tyrosine hydroxylase.

MeSH terms

  • Animals
  • Behavioral Symptoms / etiology*
  • Brain / drug effects*
  • Brain / metabolism
  • Cells, Cultured
  • Discrimination, Psychological / drug effects
  • Disease Models, Animal
  • Embryo, Mammalian
  • Humans
  • Injections, Intraventricular
  • Male
  • Maze Learning / drug effects
  • Mesencephalon / cytology
  • Mice
  • Mice, Transgenic
  • Neurons / drug effects
  • Neurons / metabolism
  • Olfaction Disorders / etiology*
  • Parkinson Disease / complications*
  • Parkinson Disease / etiology*
  • Peptides / toxicity
  • Recognition, Psychology / drug effects
  • Tyrosine 3-Monooxygenase / metabolism
  • alpha-Synuclein / chemistry
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism
  • alpha-Synuclein / toxicity*

Substances

  • Peptides
  • alpha-Synuclein
  • Tyrosine 3-Monooxygenase