Skip to main content
Erschienen in: Brain Structure and Function 2/2018

09.10.2017 | Original Article

Shaping somatosensory responses in awake rats: cortical modulation of thalamic neurons

verfasst von: Daichi Hirai, Kouichi C. Nakamura, Ken-ichi Shibata, Takuma Tanaka, Hiroyuki Hioki, Takeshi Kaneko, Takahiro Furuta

Erschienen in: Brain Structure and Function | Ausgabe 2/2018

Einloggen, um Zugang zu erhalten

Abstract

Massive corticothalamic afferents originating from layer 6a of primary sensory cortical areas modulate sensory responsiveness of thalamocortical neurons and are pivotal for shifting neuronal firing between burst and tonic modes. The influence of the corticothalamic pathways on the firing mode and sensory gain of thalamic neurons has only been extensively examined in anesthetized animals, but has yet to be established in the awake state. We made lesions of the rat barrel cortex and on the following day recorded responses of single thalamocortical and thalamic reticular neurons to a single vibrissal deflection in the somatosensory system during wakefulness. Our results showed that the cortical lesions shifted the response of thalamic neurons towards bursting, elevated the response probability and the gain of thalamocortical neurons, predominantly of recurring responses. In addition, after the lesions, the spontaneous activities of the vibrissa-responsive thalamic neurons, but not those of vibrissa-unresponsive cells, were typified by waxing-and-waning spindle-like rhythmic spiking with frequent bursting. In awake rats with intact cortex, identified layer 6a corticothalamic neurons responded to a single vibrissal deflection with short latencies that matched those of layer 4 neurons, strongly suggesting the existence of an immediate corticothalamic feedback. The present results show the importance of corticothalamic neurons in shaping thalamic activities during wakefulness.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1997) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 17:1179–1196PubMed Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1997) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 17:1179–1196PubMed
Zurück zum Zitat de Labra C, Rivadulla C, Grieve K et al (2007) Changes in visual responses in the feline dLGN: selective thalamic suppression induced by transcranial magnetic stimulation of V1. Cereb Cortex 17:1376–1385. doi:10.1093/cercor/bhl048 PubMedCrossRef de Labra C, Rivadulla C, Grieve K et al (2007) Changes in visual responses in the feline dLGN: selective thalamic suppression induced by transcranial magnetic stimulation of V1. Cereb Cortex 17:1376–1385. doi:10.​1093/​cercor/​bhl048 PubMedCrossRef
Zurück zum Zitat Diamond ME, Armstrong-James M, Budway MJ, Ebner FF (1992) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319:66–84. doi:10.1002/cne.903190108 PubMedCrossRef Diamond ME, Armstrong-James M, Budway MJ, Ebner FF (1992) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319:66–84. doi:10.​1002/​cne.​903190108 PubMedCrossRef
Zurück zum Zitat Einevoll GT, Pettersen KH, Devor A et al (2007) Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J Neurophysiol 97:2174–2190. doi:10.1152/jn.00845.2006 PubMedCrossRef Einevoll GT, Pettersen KH, Devor A et al (2007) Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J Neurophysiol 97:2174–2190. doi:10.​1152/​jn.​00845.​2006 PubMedCrossRef
Zurück zum Zitat Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379–387. doi:10.1002/cne.1037 PubMedCrossRef Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379–387. doi:10.​1002/​cne.​1037 PubMedCrossRef
Zurück zum Zitat Ghosh S, Murray GM, Turman AB, Rowe MJ (1994) Corticothalamic influences on transmission of tactile information in the ventroposterolateral thalamus of the cat: effect of reversible inactivation of somatosensory cortical areas I and II. Exp Brain Res 100:276–286. doi:10.1007/BF00227197 PubMedCrossRef Ghosh S, Murray GM, Turman AB, Rowe MJ (1994) Corticothalamic influences on transmission of tactile information in the ventroposterolateral thalamus of the cat: effect of reversible inactivation of somatosensory cortical areas I and II. Exp Brain Res 100:276–286. doi:10.​1007/​BF00227197 PubMedCrossRef
Zurück zum Zitat Guido W, Weyand T (1995) Burst responses in thalamic relay cells of the awake behaving cat. J Neurophysiol 74:1782–1786PubMedCrossRef Guido W, Weyand T (1995) Burst responses in thalamic relay cells of the awake behaving cat. J Neurophysiol 74:1782–1786PubMedCrossRef
Zurück zum Zitat Guido W, Lu SM, Sherman SM (1992) Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. J Neurophysiol 68:2199–2211PubMedCrossRef Guido W, Lu SM, Sherman SM (1992) Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. J Neurophysiol 68:2199–2211PubMedCrossRef
Zurück zum Zitat Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70 Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70
Zurück zum Zitat Kalil RE, Chase R (1970) Corticofugal influence on activity of lateral geniculate neurons in the cat. J Neurophysiol 33:459–474PubMedCrossRef Kalil RE, Chase R (1970) Corticofugal influence on activity of lateral geniculate neurons in the cat. J Neurophysiol 33:459–474PubMedCrossRef
Zurück zum Zitat Kaneko T, Caria MA, Asanuma H (1994) Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex. J Comp Neurol 345:172–184. doi:10.1002/cne.903450203 PubMedCrossRef Kaneko T, Caria MA, Asanuma H (1994) Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex. J Comp Neurol 345:172–184. doi:10.​1002/​cne.​903450203 PubMedCrossRef
Zurück zum Zitat Kaneko T, Saeki K, Lee T, Mizuno N (1996) Improved retrograde axonal transport and subsequent visualization of tetramethylrhodamine (TMR)-dextran amine by means of an acidic injection vehicle and antibodies against TMR. J Neurosci Methods 65:157–165. doi:10.1016/0165-0270(95)00162-X PubMedCrossRef Kaneko T, Saeki K, Lee T, Mizuno N (1996) Improved retrograde axonal transport and subsequent visualization of tetramethylrhodamine (TMR)-dextran amine by means of an acidic injection vehicle and antibodies against TMR. J Neurosci Methods 65:157–165. doi:10.​1016/​0165-0270(95)00162-X PubMedCrossRef
Zurück zum Zitat Kuramoto E, Furuta T, Nakamura KC et al (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065–2077. doi:10.1093/cercor/bhn231 PubMedCrossRef Kuramoto E, Furuta T, Nakamura KC et al (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065–2077. doi:10.​1093/​cercor/​bhn231 PubMedCrossRef
Zurück zum Zitat Lee SM, Friedberg MH, Ebner FF (1994) The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. I. Assessment of receptive field changes following thalamic reticular nucleus lesions. J Neurophysiol 71:1702–1715PubMedCrossRef Lee SM, Friedberg MH, Ebner FF (1994) The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. I. Assessment of receptive field changes following thalamic reticular nucleus lesions. J Neurophysiol 71:1702–1715PubMedCrossRef
Zurück zum Zitat Liu XB, Honda CN, Jones EG (1995) Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352:69–91. doi:10.1002/cne.903520106 PubMedCrossRef Liu XB, Honda CN, Jones EG (1995) Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352:69–91. doi:10.​1002/​cne.​903520106 PubMedCrossRef
Zurück zum Zitat Lo FS, Lu SM, Sherman SM (1991) Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat’s lateral geniculate nucleus. Exp Brain Res 83:317–328PubMedCrossRef Lo FS, Lu SM, Sherman SM (1991) Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat’s lateral geniculate nucleus. Exp Brain Res 83:317–328PubMedCrossRef
Zurück zum Zitat Lu SM, Guido W, Sherman SM (1992) Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. J Neurophysiol 68:2185–2198PubMedCrossRef Lu SM, Guido W, Sherman SM (1992) Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. J Neurophysiol 68:2185–2198PubMedCrossRef
Zurück zum Zitat Massaux A, Dutrieux G, Cotillon-Williams N et al (2004) Auditory thalamus bursts in anesthetized and non-anesthetized states: contribution to functional properties. J Neurophysiol 91:2117–2134. doi:10.1152/jn.00970.2003 PubMedCrossRef Massaux A, Dutrieux G, Cotillon-Williams N et al (2004) Auditory thalamus bursts in anesthetized and non-anesthetized states: contribution to functional properties. J Neurophysiol 91:2117–2134. doi:10.​1152/​jn.​00970.​2003 PubMedCrossRef
Zurück zum Zitat Maunsell JH, Gibson JR (1992) Visual response latencies in striate cortex of the macaque monkey. J Neurophysiol 68:1332–1344PubMedCrossRef Maunsell JH, Gibson JR (1992) Visual response latencies in striate cortex of the macaque monkey. J Neurophysiol 68:1332–1344PubMedCrossRef
Zurück zum Zitat McCormick DA, von Krosigk M (1992) Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc Natl Acad Sci USA 89:2774–2778PubMedPubMedCentralCrossRef McCormick DA, von Krosigk M (1992) Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc Natl Acad Sci USA 89:2774–2778PubMedPubMedCentralCrossRef
Zurück zum Zitat Morison RS, Bassett DL (1945) Electrical activity of the thalamus and basal ganglia in decorticate cats. J Neurophysiol 8:309–314CrossRef Morison RS, Bassett DL (1945) Electrical activity of the thalamus and basal ganglia in decorticate cats. J Neurophysiol 8:309–314CrossRef
Zurück zum Zitat Nakamura KC, Sharott A, Magill PJ (2014) Temporal coupling with cortex distinguishes spontaneous neuronal activities in identified basal ganglia-recipient and cerebellar-recipient zones of the motor thalamus. Cereb Cortex 24:81–97. doi:10.1093/cercor/bhs287 PubMedCrossRef Nakamura KC, Sharott A, Magill PJ (2014) Temporal coupling with cortex distinguishes spontaneous neuronal activities in identified basal ganglia-recipient and cerebellar-recipient zones of the motor thalamus. Cereb Cortex 24:81–97. doi:10.​1093/​cercor/​bhs287 PubMedCrossRef
Zurück zum Zitat Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65:113–136. doi:10.1016/0165-0270(95)00144-1 PubMedCrossRef Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65:113–136. doi:10.​1016/​0165-0270(95)00144-1 PubMedCrossRef
Zurück zum Zitat Przybyszewski AW, Gaska JP, Foote W, Pollen DA (2000) Striate cortex increases contrast gain of macaque LGN neurons. Vis Neurosci 17:485–494PubMedCrossRef Przybyszewski AW, Gaska JP, Foote W, Pollen DA (2000) Striate cortex increases contrast gain of macaque LGN neurons. Vis Neurosci 17:485–494PubMedCrossRef
Zurück zum Zitat Ramcharan EJ, Gnadt JW, Sherman SM (2000) Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis Neurosci 17:55–62PubMedCrossRef Ramcharan EJ, Gnadt JW, Sherman SM (2000) Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis Neurosci 17:55–62PubMedCrossRef
Zurück zum Zitat Rivadulla C, Martínez LM, Varela C, Cudeiro J (2002) Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J Neurosci 22:2956–2962PubMed Rivadulla C, Martínez LM, Varela C, Cudeiro J (2002) Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J Neurosci 22:2956–2962PubMed
Zurück zum Zitat Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367–1395PubMedCrossRef Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367–1395PubMedCrossRef
Zurück zum Zitat Sherman SM, Guillery RW (1998) On the actions that one nerve cell can have on another: distinguishing “drivers” from “modulators”. Proc Natl Acad Sci USA 95:7121–7126PubMedPubMedCentralCrossRef Sherman SM, Guillery RW (1998) On the actions that one nerve cell can have on another: distinguishing “drivers” from “modulators”. Proc Natl Acad Sci USA 95:7121–7126PubMedPubMedCentralCrossRef
Zurück zum Zitat Sherman SM, Guillery RW (2006) Exploring the thalamus and its role in cortical function, 2nd edn. MIT Press, Cambridge Sherman SM, Guillery RW (2006) Exploring the thalamus and its role in cortical function, 2nd edn. MIT Press, Cambridge
Zurück zum Zitat Sherman SM, Guillery RW (2013) Functional connections of cortical areas: a new view from the thalamus. MIT Press, CambridgeCrossRef Sherman SM, Guillery RW (2013) Functional connections of cortical areas: a new view from the thalamus. MIT Press, CambridgeCrossRef
Zurück zum Zitat Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798–820PubMedCrossRef Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798–820PubMedCrossRef
Zurück zum Zitat Steriade M, Deschênes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473–1497PubMedCrossRef Steriade M, Deschênes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473–1497PubMedCrossRef
Zurück zum Zitat Steriade M, Domich L, Oakson G, Deschênes M (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. J Neurophysiol 57:260–273PubMedCrossRef Steriade M, Domich L, Oakson G, Deschênes M (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. J Neurophysiol 57:260–273PubMedCrossRef
Zurück zum Zitat Timofeev I, Bazhenov M, Seigneur J, Sejnowski T (2012) Neuronal synchronization and thalamocortical rhythms in sleep, wake and epilepsy. In: Noebels JL, Avoli M, Rogawski MA et al (eds) Jasper’s basic mechanisms of the epilepsies, 4th edn. National Center for Biotechnology Information, Bethesda Timofeev I, Bazhenov M, Seigneur J, Sejnowski T (2012) Neuronal synchronization and thalamocortical rhythms in sleep, wake and epilepsy. In: Noebels JL, Avoli M, Rogawski MA et al (eds) Jasper’s basic mechanisms of the epilepsies, 4th edn. National Center for Biotechnology Information, Bethesda
Zurück zum Zitat Varga C, Sík A, Lavallée P, Deschênes M (2002) Dendroarchitecture of relay cells in thalamic barreloids: a substrate for cross-whisker modulation. J Neurosci 22:6186–6194PubMed Varga C, Sík A, Lavallée P, Deschênes M (2002) Dendroarchitecture of relay cells in thalamic barreloids: a substrate for cross-whisker modulation. J Neurosci 22:6186–6194PubMed
Zurück zum Zitat Weyand TG, Boudreaux M, Guido W (2001) Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J Neurophysiol 85:1107–1118PubMedCrossRef Weyand TG, Boudreaux M, Guido W (2001) Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J Neurophysiol 85:1107–1118PubMedCrossRef
Zurück zum Zitat Zhan XJ, Cox CL, Rinzel J, Sherman SM (1999) Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat’s lateral geniculate nucleus. J Neurophysiol 81:2360–2373PubMedCrossRef Zhan XJ, Cox CL, Rinzel J, Sherman SM (1999) Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat’s lateral geniculate nucleus. J Neurophysiol 81:2360–2373PubMedCrossRef
Metadaten
Titel
Shaping somatosensory responses in awake rats: cortical modulation of thalamic neurons
verfasst von
Daichi Hirai
Kouichi C. Nakamura
Ken-ichi Shibata
Takuma Tanaka
Hiroyuki Hioki
Takeshi Kaneko
Takahiro Furuta
Publikationsdatum
09.10.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 2/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1522-z

Weitere Artikel der Ausgabe 2/2018

Brain Structure and Function 2/2018 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.