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Published in: Brain Structure and Function 3/2018

01-04-2018 | Original Article

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

Authors: M. A. Arias-García, D. Tapia, J. A. Laville, V. M. Calderón, Y. Ramiro-Cortés, J. Bargas, E. Galarraga

Published in: Brain Structure and Function | Issue 3/2018

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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.
Literature
go back to reference Bennett BD, Wilson CJ (1999) Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586–5596PubMed Bennett BD, Wilson CJ (1999) Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586–5596PubMed
go back to reference Castle M, Aymerich MS, Sanchez-Escobar C, Gonzalo N, Obeso JA, Lanciego JL (2005) Thalamic innervation of the direct and indirect basal ganglia pathways in the rat: ipsi- and contralateral projections. J Comp Neurol 483:143–153. doi:10.1002/cne.20421 PubMedCrossRef Castle M, Aymerich MS, Sanchez-Escobar C, Gonzalo N, Obeso JA, Lanciego JL (2005) Thalamic innervation of the direct and indirect basal ganglia pathways in the rat: ipsi- and contralateral projections. J Comp Neurol 483:143–153. doi:10.​1002/​cne.​20421 PubMedCrossRef
go back to reference Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17–32PubMedCrossRef Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17–32PubMedCrossRef
go back to reference Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455–471. doi:10.1002/cne.902670402 PubMedCrossRef Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455–471. doi:10.​1002/​cne.​902670402 PubMedCrossRef
go back to reference English DF, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsaki G, Deisseroth K, Tepper JM, Koos T (2011) GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 15:123–130. doi:10.1038/nn.2984 PubMedPubMedCentralCrossRef English DF, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsaki G, Deisseroth K, Tepper JM, Koos T (2011) GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 15:123–130. doi:10.​1038/​nn.​2984 PubMedPubMedCentralCrossRef
go back to reference 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 PubMedPubMedCentralCrossRef 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 PubMedPubMedCentralCrossRef
go back to reference Flores-Barrera E, Laville A, Plata V, Tapia D, Bargas J, Galarraga E (2009) Inhibitory contribution to suprathreshold corticostriatal responses: an experimental and modeling study. Cell Mol Neurobiol 29:719–731. doi:10.1007/s10571-009-9394-2 PubMedCrossRef Flores-Barrera E, Laville A, Plata V, Tapia D, Bargas J, Galarraga E (2009) Inhibitory contribution to suprathreshold corticostriatal responses: an experimental and modeling study. Cell Mol Neurobiol 29:719–731. doi:10.​1007/​s10571-009-9394-2 PubMedCrossRef
go back to reference Fujiyama F, Unzai T, Nakamura K, Nomura S, Kaneko T (2006) Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur J Neurosci 24:2813–2824PubMedCrossRef Fujiyama F, Unzai T, Nakamura K, Nomura S, Kaneko T (2006) Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur J Neurosci 24:2813–2824PubMedCrossRef
go back to reference Hunnicutt BJ, Jongbloets BC, Birdsong WT, Gertz KJ, Zhong H, Mao T (2016) A comprehensive excitatory input map of the striatum reveals novel functional organization. Elife 28:5. doi:10.7554/eLife.19103 Hunnicutt BJ, Jongbloets BC, Birdsong WT, Gertz KJ, Zhong H, Mao T (2016) A comprehensive excitatory input map of the striatum reveals novel functional organization. Elife 28:5. doi:10.​7554/​eLife.​19103
go back to reference Jahnsen H, Llinás R (1984) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227–247PubMedPubMedCentralCrossRef Jahnsen H, Llinás R (1984) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227–247PubMedPubMedCentralCrossRef
go back to reference Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923PubMed Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923PubMed
go back to reference Lambe EK, Aghajanian GK (2007) Prefrontal cortical network activity: opposite effects of psychodelic hallucinogens and D1/D5 dopamine receptor activation. Neuroscience 145:900–910PubMedPubMedCentralCrossRef Lambe EK, Aghajanian GK (2007) Prefrontal cortical network activity: opposite effects of psychodelic hallucinogens and D1/D5 dopamine receptor activation. Neuroscience 145:900–910PubMedPubMedCentralCrossRef
go back to reference Macchi G, Bentivoglio M, Molinari M, Minciacchi D (1984) The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp Brain Res 54:225–239PubMedCrossRef Macchi G, Bentivoglio M, Molinari M, Minciacchi D (1984) The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp Brain Res 54:225–239PubMedCrossRef
go back to reference Malliani A, Purpura DP (1967) Patterns of synaptic activities in lenticular and entopeduncular neurons. Brain Res 6:341–354PubMedCrossRef Malliani A, Purpura DP (1967) Patterns of synaptic activities in lenticular and entopeduncular neurons. Brain Res 6:341–354PubMedCrossRef
go back to reference Marco LA, Copack P, Edelson AM (1973) Intrinsic connections of caudate neurons. Locally evoked intracellular responses. Exp Neurol 40:683–698PubMedCrossRef Marco LA, Copack P, Edelson AM (1973) Intrinsic connections of caudate neurons. Locally evoked intracellular responses. Exp Neurol 40:683–698PubMedCrossRef
go back to reference Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM–Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976PubMedCrossRef Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM–Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976PubMedCrossRef
go back to reference 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 PubMedCrossRef 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 PubMedCrossRef
go back to reference Minamimoto T, Hori Y, Kimura M (2005) Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308:1798–1801PubMedCrossRef Minamimoto T, Hori Y, Kimura M (2005) Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308:1798–1801PubMedCrossRef
go back to reference Muñoz-Manchado AB, Foldi C, Szydlowski S, Sjulson L, Farries M, Wilson C, Silberberg G, Hjerling-Leffler J (2016) Novel striatal GABAergic interneuron populations labeled in the 5HT3a (EGFP) mouse. Cereb Cortex 26:96–105. doi:10.1093/cercor/bhu179 PubMedCrossRef Muñoz-Manchado AB, Foldi C, Szydlowski S, Sjulson L, Farries M, Wilson C, Silberberg G, Hjerling-Leffler J (2016) Novel striatal GABAergic interneuron populations labeled in the 5HT3a (EGFP) mouse. Cereb Cortex 26:96–105. doi:10.​1093/​cercor/​bhu179 PubMedCrossRef
go back to reference 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 PubMedCrossRef 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 PubMedCrossRef
go back to reference Purpura DP, Malliani A (1967) I. Synaptic potentials and discharge characteristics of caudate neurons activated by thalamic stimulation. Brain Res 6:325–340PubMedCrossRef Purpura DP, Malliani A (1967) I. Synaptic potentials and discharge characteristics of caudate neurons activated by thalamic stimulation. Brain Res 6:325–340PubMedCrossRef
go back to reference Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138–1168PubMedCrossRef Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138–1168PubMedCrossRef
go back to reference Rall W, Burke RE, Holmes WR, Jack JJB, Redman SJ, Segev I (1992) Matching dendritic neuron models to experimental data. Physiol Rev 72:159–186CrossRef Rall W, Burke RE, Holmes WR, Jack JJB, Redman SJ, Segev I (1992) Matching dendritic neuron models to experimental data. Physiol Rev 72:159–186CrossRef
go back to reference Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158–8169PubMed Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158–8169PubMed
go back to reference Reyes A, Galarraga E, Flores-Hernández J, Tapia D, Bargas J (1998) Passive properties of neostriatal neurons during potassium conductance blockade. Exp Brain Res 120:70–84PubMedCrossRef Reyes A, Galarraga E, Flores-Hernández J, Tapia D, Bargas J (1998) Passive properties of neostriatal neurons during potassium conductance blockade. Exp Brain Res 120:70–84PubMedCrossRef
go back to reference Schlösser B, ten Bruggencate G, Sutor B (1999) Local disinhibition of neocortical neuronal circuits causes augmentation of glutamatergic and GABAergic synaptic transmission in the rat neostriatum in vitro. Exp Neurol 157:180–193PubMedCrossRef Schlösser B, ten Bruggencate G, Sutor B (1999) Local disinhibition of neocortical neuronal circuits causes augmentation of glutamatergic and GABAergic synaptic transmission in the rat neostriatum in vitro. Exp Neurol 157:180–193PubMedCrossRef
go back to reference Sciamanna G, Ponterio G, Mandolesi G, Bonsi P, Pisani A (2015) Optogenetic stimulation reveals distinct modulatory properties of thalamostriatal vs corticostriatal glutamatergic inputs to fast spiking interneurons. Sci Rep 5:16742. doi:10.1038/srep16742 PubMedPubMedCentralCrossRef Sciamanna G, Ponterio G, Mandolesi G, Bonsi P, Pisani A (2015) Optogenetic stimulation reveals distinct modulatory properties of thalamostriatal vs corticostriatal glutamatergic inputs to fast spiking interneurons. Sci Rep 5:16742. doi:10.​1038/​srep16742 PubMedPubMedCentralCrossRef
go back to reference Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77(4):1697–1715 (PMID: 9114230) PubMedCrossRef Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77(4):1697–1715 (PMID: 9114230) PubMedCrossRef
go back to reference Vergara R, Rick C, Hernández- López S, Laville JA, Guzman JN, Galarraga E, Surmeier DJ, Bargas J (2003) Spontaneous voltage oscillations in striatal projection neurons in a rat cortico striatal slice. J Physiol 15:169–182. doi:10.1113/jphysiol.2003.050799 CrossRef Vergara R, Rick C, Hernández- López S, Laville JA, Guzman JN, Galarraga E, Surmeier DJ, Bargas J (2003) Spontaneous voltage oscillations in striatal projection neurons in a rat cortico striatal slice. J Physiol 15:169–182. doi:10.​1113/​jphysiol.​2003.​050799 CrossRef
go back to reference 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 PubMedPubMedCentralCrossRef 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 PubMedPubMedCentralCrossRef
go back to reference Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397–2410PubMed Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397–2410PubMed
go back to reference Wilson CJ, Chang HT, Kitai ST (1990) Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10:508–519PubMed Wilson CJ, Chang HT, Kitai ST (1990) Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10:508–519PubMed
Metadata
Title
Functional comparison of corticostriatal and thalamostriatal postsynaptic responses in striatal neurons of the mouse
Authors
M. A. Arias-García
D. Tapia
J. A. Laville
V. M. Calderón
Y. Ramiro-Cortés
J. Bargas
E. Galarraga
Publication date
01-04-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1536-6

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