Widespread optogenetic expression in macaque cortex obtained with MR-guided, convection enhanced delivery (CED) of AAV vector to the thalamus

J Neurosci Methods. 2018 Jan 1:293:347-358. doi: 10.1016/j.jneumeth.2017.10.009. Epub 2017 Oct 16.

Abstract

Background: In non-human primate (NHP) optogenetics, infecting large cortical areas with viral vectors is often a difficult and time-consuming task. Previous work has shown that parenchymal delivery of adeno-associated virus (AAV) in the thalamus by convection-enhanced delivery (CED) can lead to large-scale transduction via axonal transport in distal areas including cortex. We used this approach to obtain widespread cortical expression of light-sensitive ion channels.

New method: AAV vectors co-expressing channelrhodopsin-2 (ChR2) and yellow fluorescent protein (YFP) genes were infused into thalamus of three rhesus macaques under MR-guided CED. After six to twelve weeks recovery, in vivo optical stimulation and single cell recording in the cortex was carried out using an optrode in anesthetized animals. Post-mortem immunostaining against YFP was used to estimate the distribution and level of expression of ChR2 in thalamus and cortex.

Results: Histological analysis revealed high levels of transduction in cortical layers. The patterns of expression were consistent with known thalamo-cortico-thalamic circuits. Dense expression was seen in thalamocortiocal axonal fibers in layers III, IV and VI and in pyramidal neurons in layers V and VI, presumably corticothalamic neurons. In addition we obtained reliable in vivo light-evoked responses in cortical areas with high levels of expression.

Comparison with existing methods: Thalamic CED is very efficient in achieving large expressing areas in comparison to convectional techniques both in minimizing infusion time and in minimizing damage to the brain.

Conclusion: MR-guided CED infusion into thalamus provides a simplified approach to transduce large cortical areas by thalamo-cortico-thalamic projections in primate brain.

Keywords: Non-human primates; Opsin expression; Optogenetics; Sensorimotor cortex; Thalamo-cortical pathway; Viral vector delivery.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cerebral Cortex / cytology
  • Cerebral Cortex / diagnostic imaging
  • Cerebral Cortex / physiology
  • Channelrhodopsins / genetics
  • Channelrhodopsins / metabolism
  • Convection
  • Dependovirus / genetics*
  • Dermoscopy
  • Female
  • Genetic Vectors / administration & dosage*
  • Imaging, Three-Dimensional
  • Immunohistochemistry
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Macaca mulatta*
  • Magnetic Resonance Imaging
  • Male
  • Models, Animal
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Optogenetics / methods*
  • Photic Stimulation
  • Thalamus* / cytology
  • Thalamus* / diagnostic imaging
  • Thalamus* / physiology

Substances

  • Bacterial Proteins
  • Channelrhodopsins
  • Luminescent Proteins
  • yellow fluorescent protein, Bacteria