Functional comparison of corticostriatal and thalamostriatal postsynaptic responses in striatal neurons of the mouse
- 499 Downloads
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.
KeywordsStriatum Striatal projection neurons Striatal interneurons Synaptic integration Intrinsic properties Corticostriatal pathway Thalamostriatal pathway
We thank Gabriela X Ayala and Ariadna Aparicio for technical support and advice and Dr. Claudia Rivera for animal care. We thank Dr. Rene Druker-Colín for his help with transgenic animals. This work was supported by Consejo Nacional de Ciencia y Tecnología (México) Grant Frontera 57 to JB and 251144 to EG, and by Grants from Dirección General de Asuntos del Personal Académico. Universidad Nacional Autónoma de México: IN201417 and IN201517 to JB and EG. Mario A. Arias-García had a DGAPA and CONACyT doctoral fellowships and data in this work are part of his doctoral dissertation in the Doctorado en Ciencias Biomédicas de la Universidad Nacional Autónoma de México.
- Arias-García MA, Tapia D, Flores-Barrera E, Pérez-Ortega JE, Bargas J, Galarraga E (2013) Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents. Front Syst Neurosci 7:63. doi: 10.3389/fnsys.2013.00063 PubMedPubMedCentralCrossRefGoogle Scholar
- Doig NM, Magill PJ, Apicella P, Bolam JP, Sharott A (2014) Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic Interneurons to motivationally salient stimuli. J Neurosci 34:3101–3117. doi: 10.1523/JNEUROSCI.4627-13.2014 PubMedPubMedCentralCrossRefGoogle Scholar
- Fieblinger T, Graves SM, Sebel LE, Alcacer C, Plotkin JL, Gertler TS, Chan CS, Heiman M, Greengard P, Cenci MA, Surmeier DJ (2014) Cell type-specific plasticity of striatal projection neurons in parkinsonism and l-DOPA-induced dyskinesia. Nat Commun 5:5316. doi: 10.1038/ncomms6316 PubMedPubMedCentralCrossRefGoogle Scholar
- Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koos T, Tepper JM (2010) Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J Neurosci 30:6999–7016. doi: 10.1523/JNEUROSCI.5996-09.2010 PubMedPubMedCentralCrossRefGoogle Scholar
- Maurice N, Liberge M, Jaouen F, Ztaou S, Hanini M, Camon J, Deisseroth K, Amalric M, Kerkerian-Le Goff L, Beurrier C (2015) Striatal cholinergic interneurons control motor behavior and basal ganglia function in experimental parkinsonism. Cell Rep 13:657–666. doi: 10.1016/j.celrep.2015.09.034 PubMedCrossRefGoogle Scholar
- Pérez-Ortega J, Duhne M, Lara-Gonzalez E, Plata V, Gasca D, Galarraga E, Hernández-Cruz A, Bargas J (2016) Pathophysiological signatures of functional connectomics in parkinsonian and dyskinetic striatal microcircuits. Neurobiol Dis 91:347–361. doi: 10.1016/j.nbd.2016.02.023 PubMedCrossRefGoogle Scholar
- Sciamanna G, Tassone A, Mandolesi G, Puglisi F, Ponterio G, Martella G, Madeo G, Bernardi G, Standaert DG, Bonsi P, Pisani C (2012) Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J Neurosci 32:11991–12004. doi: 10.1523/JNEUROSCI.0041-12.2012 PubMedPubMedCentralCrossRefGoogle Scholar
- Thomas TM, Smith Y, Levey AI, Hersch SM (2000) Cortical inputs to m2-immunoreactive striatal interneurons in rat and monkey. Synapse 37:252–261. doi: 10.1002/1098-2396(20000915)37:4<252:AID-SYN2>3.0.CO;2-A PubMedCrossRefGoogle Scholar
- Vizcarra-Chacón B, Arias-García MA, Pérez-Ramirez MB, Flores-Barrera E, Tapia D, Drucker-Colin R, Bargas J, Galarraga E (2013) Contribution of different classes of glutamate receptors in the cortico-striatal polysynaptic responses from striatal direct and indirect projection neurons. BMC Neurosci 14:60. doi: 10.1186/1471-2202-14-60 PubMedPubMedCentralCrossRefGoogle Scholar