Functional comparison of corticostriatal and thalamostriatal postsynaptic responses in striatal neurons of the mouse

Brain Struct Funct. 2018 Apr;223(3):1229-1253. doi: 10.1007/s00429-017-1536-6. Epub 2017 Nov 3.

Abstract

Synaptic inputs from cortex and thalamus were compared in electrophysiologically defined striatal cell classes: direct and indirect pathways' striatal projection neurons (dSPNs and iSPNs), fast-spiking interneurons (FS), cholinergic interneurons (ChINs), and low-threshold spiking-like (LTS-like) interneurons. Our purpose was to observe whether stimulus from cortex or thalamus had equivalent synaptic strength to evoke prolonged suprathreshold synaptic responses in these neuron classes. Subthreshold responses showed that inputs from either source functionally mix up in their dendrites at similar electrotonic distances from their somata. Passive and active properties of striatal neuron classes were consistent with the previous studies. Cre-dependent adeno-associated viruses containing Td-Tomato or eYFP fluorescent proteins were used to identify target cells. Transfections with ChR2-eYFP driven by the promoters CamKII or EF1.DIO in intralaminar thalamic nuclei using Vglut-2-Cre mice, or CAMKII in the motor cortex were used to stimulate cortical or thalamic afferents optogenetically. Both field stimuli in the cortex or photostimulation of ChR2-YFP cortical fibers evoked similar prolonged suprathreshold responses in SPNs. Photostimulation of ChR2-YFP thalamic afferents also evoked suprathreshold responses. Differences previously described between responses of dSPNs and iSPNs were observed in both cases. Prolonged suprathreshold responses could also be evoked from both sources onto all other neuron classes studied. However, to evoke thalamostriatal suprathreshold responses, afferents from more than one thalamic nucleus had to be stimulated. In conclusion, both thalamus and cortex are capable to generate suprathreshold responses converging on diverse striatal cell classes. Postsynaptic properties appear to shape these responses.

Keywords: Corticostriatal pathway; Intrinsic properties; Striatal interneurons; Striatal projection neurons; Striatum; Synaptic integration; Thalamostriatal pathway.

MeSH terms

  • Analysis of Variance
  • Animals
  • Cerebral Cortex / physiology*
  • Choline O-Acetyltransferase / metabolism
  • Corpus Striatum / cytology*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Lysine / analogs & derivatives
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neural Pathways / drug effects
  • Neural Pathways / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Synaptic Potentials / drug effects
  • Synaptic Potentials / physiology*
  • Thalamus / physiology*
  • Vesicular Glutamate Transport Protein 2 / genetics
  • Vesicular Glutamate Transport Protein 2 / metabolism

Substances

  • Excitatory Amino Acid Antagonists
  • Luminescent Proteins
  • Nerve Tissue Proteins
  • Slc17a6 protein, mouse
  • Vesicular Glutamate Transport Protein 2
  • Choline O-Acetyltransferase
  • biocytin
  • Lysine