Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex.
The thalamus provides fundamental input to the neocortex. This input activates inhibitory interneurons more strongly than excitatory neurons, triggering powerful feedforward inhibition. We studied the mechanisms of this selective neuronal activation using a mouse somatosensory thalamocortical preparation. Notably, the greater responsiveness of inhibitory interneurons was not caused by their distinctive intrinsic properties but was instead produced by synaptic mechanisms. Axons from the thalamus made stronger and more frequent excitatory connections onto inhibitory interneurons than onto excitatory cells. Furthermore, circuit dynamics allowed feedforward inhibition to suppress responses in excitatory cells more effectively than in interneurons. Thalamocortical excitatory currents rose quickly in interneurons, allowing them to fire action potentials before significant feedforward inhibition emerged. In contrast, thalamocortical excitatory currents rose slowly in excitatory cells, overlapping with feedforward inhibitory currents that suppress action potentials. These results demonstrate the importance of selective synaptic targeting and precise timing in the initial stages of neocortical processing.
Cruikshank
Scott J
SJ
Department of Neuroscience, Division of Biology & Medicine, Box G-LN, Brown University, Providence, Rhode Island 02912, USA.
Lewis
Timothy J
TJ
Connors
Barry W
BW
D000818:Animals; D000831:Animals, Newborn; D004307:Dose-Response Relationship, Radiation; D004558:Electric Stimulation / Q000379:methods; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology / Q000528:radiation effects; D049452:Green Fluorescent Proteins / Q000096:biosynthesis; D066298:In Vitro Techniques; D008564:Membrane Potentials / Q000502:physiology / Q000528:radiation effects; D051379:Mice; D008813:Mice, Inbred ICR; D008822:Mice, Transgenic; D019579:Neocortex / Q000166:cytology*; D009433:Neural Inhibition / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D018408:Patch-Clamp Techniques; D013569:Synapses / Q000502:physiology*; D013788:Thalamus / Q000502:physiology*
D049452:Green Fluorescent Proteins