Translaminar Cortical Membrane Potential Synchrony in Behaving Mice

• Published in: Cell reports (Cambridge) 2016-06, Vol.15 (11), p.2387-2399
• Main Authors: Zhao, Wen-Jie, Kremkow, Jens, Poulet, James F.A.
• Format: Article
• Language: English
• Subjects: Animals; Behavior, Animal - physiology; Extremities - physiology; Membrane Potentials - physiology; Mice; Movement - physiology; Physical Stimulation; Pyramidal Cells - physiology; Somatosensory Cortex - cytology; Somatosensory Cortex - physiology; Synapses - physiology; Touch; Wakefulness
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2016.05.026

The synchronized activity of six layers of cortical neurons is critical for sensory perception and the control of voluntary behavior, but little is known about the synaptic mechanisms of cortical synchrony across layers in behaving animals. We made single and dual whole-cell recordings from the primary somatosensory forepaw cortex in awake mice and show that L2/3 and L5 excitatory neurons have layer-specific intrinsic properties and membrane potential dynamics that shape laminar-specific firing rates and subthreshold synchrony. First, while sensory and movement-evoked synaptic input was tightly correlated across layers, spontaneous action potentials and slow spontaneous subthreshold fluctuations had laminar-specific timing; second, longer duration forepaw movement was associated with a decorrelation of subthreshold activity; third, spontaneous and sensory-evoked forepaw movements were signaled more strongly by L5 than L2/3 neurons. Together, our data suggest that the degree of translaminar synchrony is dependent upon the origin (sensory, spontaneous, and movement) of the synaptic input. [Display omitted] •We made dual whole-cell recordings from L2/3 and L5 cortical neurons in behaving mice•Layer-specific membrane properties determine higher mean firing rates of L5 neurons•Synchrony of translaminar synaptic activity is determined by the origin of input•L5 neurons signal spontaneous and sensory-triggered movements Zhao et al. use dual whole-cell recordings from primary somatosensory cortical excitatory neurons in layers 2/3 and 5 in awake mice to identify layer-specific cellular properties and firing rates, and they show that translaminar membrane potential synchrony is dependent both on behavioral state and the source of the synaptic input.