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Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro.
J Neurophysiol. 1997 May; 77(5):2661-76.JN

Abstract

Whole cell current- and voltage-clamp recording techniques were employed in a rat thalamocortical slice preparation to characterize corticothalamic stimulation-evoked responses in thalamic neurons. Three types of corticothalamic stimulation-evoked responses were observed in thalamic neurons. Of thalamic neurons, 57% responded to corticothalamic stimulation with purely excitatory synaptic responses, whereas 27% had inhibitory synaptic responses and 16% had mixed excitatory/inhibitory responses. This suggested corticothalamic activation of multiple distinct synaptic circuits, presumably involving both nucleus reticularis thalami (NRT) and thalamus, because the rat ventrobasal complex is virtually devoid of GABAergic interneurons. Corticothalamic-stimulation-evoked excitatory postsynaptic currents (EPSCs) were predominantly slow rising currents that showed nonlinear voltage dependence, characteristics of an N-methyl-D-aspartate (NMDA)-receptor-mediated synaptic current. These slow rising EPSCs were blocked by the NMDA antagonist 2-amino-5-phosphonovaleric acid (APV). A minority of corticothalamic EPSCs had faster kinetics, and were blocked by 6-cyano-7 nitroquinoxaline-2,3-dione (CNQX). Corticothalamic stimulation of varying frequency optimally activated burst responses in thalamic neurons at low frequencies (3-6 Hz). The optimal 3- to 6-Hz response was reduced by ethosuximide, by APV, and by detaching the neocortex from the thalamocortical slice, suggesting that T current, NMDA receptors, and neocortical properties all contributed to generation of this 3- to 6-Hz frequency preference. In contrast to corticothalamic EPSCs, medial-thalamic-stimulation-evoked responses consisted of fast CNQX-sensitive EPSCs that were predominantly voltage insensitive, with no 3- to 6-Hz frequency preference. In thalamic neurons in which corticothalamic stimulation evoked predominantly inhibitory synaptic responses, this inhibitory postsynaptic potential (IPSP) had early and late phases, often followed by a rebound burst. The early IPSP reversed at -95 mV and was bicuculline sensitive, whereas the late IPSP reversed at -113 mV and was blocked by the gamma-aminobutyric acid-B (GABA(B)) antagonist 3-N[1-(S)-(3,4-dichlorophenyl)ethyl]amino-2-(S)-hydroxypropyl-P-benzy lphoshinic acid (CGP-55845A). In thalamic neurons in which corticothalamic stimulation evoked a mixed excitatory postsynaptic potential (EPSP)/IPSP response, repetitive corticothalamic stimulation rapidly reduced IPSPs and enhanced EPSPs at higher frequencies. This resulted in burst firing being triggered in these mixed response neurons at frequencies >6 Hz. Corticothalamic feedback onto thalamic relay neurons activated diverse responses due to differing relative activation of NRT and "feedforward" inhibitory responses. These multiple in vitro corticothalamic responses differ from responses encountered in other in vitro thalamic preparations lacking a synaptically connected neocortex, but are similar to results evident in thalamic neurons in response to cortical stimulation in vivo. In addition, the thalamocortical 3- to 6-Hz frequency preference was conserved, suggesting that many factors critical for this emergent property of the thalamocortical system are maintained in vitro.

Authors+Show Affiliations

Department of Neurology, Medical College of Virginia, Richmond 23298-0599, USA.No affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

9163382

Citation

Kao, C Q., and D A. Coulter. "Physiology and Pharmacology of Corticothalamic Stimulation-evoked Responses in Rat Somatosensory Thalamic Neurons in Vitro." Journal of Neurophysiology, vol. 77, no. 5, 1997, pp. 2661-76.
Kao CQ, Coulter DA. Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. J Neurophysiol. 1997;77(5):2661-76.
Kao, C. Q., & Coulter, D. A. (1997). Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. Journal of Neurophysiology, 77(5), 2661-76.
Kao CQ, Coulter DA. Physiology and Pharmacology of Corticothalamic Stimulation-evoked Responses in Rat Somatosensory Thalamic Neurons in Vitro. J Neurophysiol. 1997;77(5):2661-76. PubMed PMID: 9163382.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. AU - Kao,C Q, AU - Coulter,D A, PY - 1997/5/1/pubmed PY - 1997/5/1/medline PY - 1997/5/1/entrez SP - 2661 EP - 76 JF - Journal of neurophysiology JO - J Neurophysiol VL - 77 IS - 5 N2 - Whole cell current- and voltage-clamp recording techniques were employed in a rat thalamocortical slice preparation to characterize corticothalamic stimulation-evoked responses in thalamic neurons. Three types of corticothalamic stimulation-evoked responses were observed in thalamic neurons. Of thalamic neurons, 57% responded to corticothalamic stimulation with purely excitatory synaptic responses, whereas 27% had inhibitory synaptic responses and 16% had mixed excitatory/inhibitory responses. This suggested corticothalamic activation of multiple distinct synaptic circuits, presumably involving both nucleus reticularis thalami (NRT) and thalamus, because the rat ventrobasal complex is virtually devoid of GABAergic interneurons. Corticothalamic-stimulation-evoked excitatory postsynaptic currents (EPSCs) were predominantly slow rising currents that showed nonlinear voltage dependence, characteristics of an N-methyl-D-aspartate (NMDA)-receptor-mediated synaptic current. These slow rising EPSCs were blocked by the NMDA antagonist 2-amino-5-phosphonovaleric acid (APV). A minority of corticothalamic EPSCs had faster kinetics, and were blocked by 6-cyano-7 nitroquinoxaline-2,3-dione (CNQX). Corticothalamic stimulation of varying frequency optimally activated burst responses in thalamic neurons at low frequencies (3-6 Hz). The optimal 3- to 6-Hz response was reduced by ethosuximide, by APV, and by detaching the neocortex from the thalamocortical slice, suggesting that T current, NMDA receptors, and neocortical properties all contributed to generation of this 3- to 6-Hz frequency preference. In contrast to corticothalamic EPSCs, medial-thalamic-stimulation-evoked responses consisted of fast CNQX-sensitive EPSCs that were predominantly voltage insensitive, with no 3- to 6-Hz frequency preference. In thalamic neurons in which corticothalamic stimulation evoked predominantly inhibitory synaptic responses, this inhibitory postsynaptic potential (IPSP) had early and late phases, often followed by a rebound burst. The early IPSP reversed at -95 mV and was bicuculline sensitive, whereas the late IPSP reversed at -113 mV and was blocked by the gamma-aminobutyric acid-B (GABA(B)) antagonist 3-N[1-(S)-(3,4-dichlorophenyl)ethyl]amino-2-(S)-hydroxypropyl-P-benzy lphoshinic acid (CGP-55845A). In thalamic neurons in which corticothalamic stimulation evoked a mixed excitatory postsynaptic potential (EPSP)/IPSP response, repetitive corticothalamic stimulation rapidly reduced IPSPs and enhanced EPSPs at higher frequencies. This resulted in burst firing being triggered in these mixed response neurons at frequencies >6 Hz. Corticothalamic feedback onto thalamic relay neurons activated diverse responses due to differing relative activation of NRT and "feedforward" inhibitory responses. These multiple in vitro corticothalamic responses differ from responses encountered in other in vitro thalamic preparations lacking a synaptically connected neocortex, but are similar to results evident in thalamic neurons in response to cortical stimulation in vivo. In addition, the thalamocortical 3- to 6-Hz frequency preference was conserved, suggesting that many factors critical for this emergent property of the thalamocortical system are maintained in vitro. SN - 0022-3077 UR - https://www.unboundmedicine.com/medline/citation/9163382/Physiology_and_pharmacology_of_corticothalamic_stimulation_evoked_responses_in_rat_somatosensory_thalamic_neurons_in_vitro_ L2 - https://journals.physiology.org/doi/10.1152/jn.1997.77.5.2661?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -