A corticothalamic switch: controlling the thalamus with dynamic synapses.
Corticothalamic neurons provide massive input to the thalamus. This top-down projection may allow the cortex to regulate sensory processing by modulating the excitability of thalamic cells. Layer 6 corticothalamic neurons monosynaptically excite thalamocortical cells, but also indirectly inhibit them by driving inhibitory cells of the thalamic reticular nucleus. Whether corticothalamic activity generally suppresses or excites the thalamus remains unclear. Here we show that the corticothalamic influence is dynamic, with the excitatory-inhibitory balance shifting in an activity-dependent fashion. During low-frequency activity, corticothalamic effects are mainly suppressive, whereas higher-frequency activity (even a short bout of gamma frequency oscillations) converts the corticothalamic influence to enhancement. The mechanism of this switching depends on distinct forms of short-term synaptic plasticity across multiple corticothalamic circuit components. Our results reveal an activity-dependent mechanism by which corticothalamic neurons can bidirectionally switch the excitability and sensory throughput of the thalamus, possibly to meet changing behavioral demands.
Department of Neuroscience, Brown University, 185 Meeting Street, Box G-LN, Providence, RI 02912, USA.
Shane R
SR
Crandall
Department of Neuroscience, Brown University, 185 Meeting Street, Box G-LN, Providence, RI 02912, USA.
Scott J
SJ
Cruikshank
Department of Neuroscience, Brown University, 185 Meeting Street, Box G-LN, Providence, RI 02912, USA. Electronic address: bc@brown.edu.
Barry W
BW
Connors
D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D000697:Central Nervous System Stimulants / Q000494:pharmacology; D000075402:Channelrhodopsins; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology*; D066298:In Vitro Techniques; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D051379:Mice; D008813:Mice, Inbred ICR; D008822:Mice, Transgenic; D016202:N-Methylaspartate / Q000494:pharmacology; D009434:Neural Pathways / Q000502:physiology*; D062308:Optogenetics; D010852:Picrotoxin / Q000494:pharmacology; D018028:Receptors, Neurotensin / Q000235:genetics / Q000378:metabolism; D013003:Somatosensory Cortex / Q000502:physiology*; D013569:Synapses / Q000235:genetics / Q000502:physiology*; D013788:Thalamus / Q000502:physiology*; D014633:Valine / Q000031:analogs & derivatives / Q000494:pharmacology; D005680:gamma-Aminobutyric Acid / Q000494:pharmacology
D001426:Bacterial Proteins; D000697:Central Nervous System Stimulants; D000075402:Channelrhodopsins; D018691:Excitatory Amino Acid Antagonists; D008164:Luminescent Proteins; D016202:N-Methylaspartate; D010852:Picrotoxin; D018028:Receptors, Neurotensin; D014633:Valine; D005680:gamma-Aminobutyric Acid; C114036:neurotensin type 1 receptor; C054562:yellow fluorescent protein, Bacteria; C056639:2-amino-5-phosphopentanoic acid