Spatiotemporal Dynamics of Sensory Responses in Layer 2/3 of Rat Barrel Cortex Measured In Vivo by Voltage-Sensitive Dye Imaging Combined with Whole-Cell Voltage Recordings and Neuron Reconstructions

Abstract

The spatiotemporal dynamics of the sensory response in layer 2/3 of primary somatosensory cortex evoked by a single brief whisker deflection was investigated by simultaneous voltage-sensitive dye (VSD) imaging and whole-cell (WC) voltage recordings in the anesthetized rat combined with reconstructions of dendritic and axonal arbors of L2/3 pyramids. Single and dual WC recordings from pyramidal cells indicated a strong correlation between the local VSD population response and the simultaneously measured subthreshold postsynaptic potential changes in both amplitude and time course. The earliest VSD response was detected 10-12 msec after whisker deflection centered above the barrel isomorphic to the stimulated principal whisker. It was restricted horizontally to the size of a single barrel-column coextensive with the dendritic arbor of barrel-column-related pyramids in L2/3. The horizontal spread of excitation remained confined to a single barrel-column with weak whisker deflection. With intermediate deflections, excitation spread into adjacent barrel-columns, propagating twofold more rapidly along the rows of the barrel field than across the arcs, consistent with the preferred axonal arborizations in L2/3 of reconstructed pyramidal neurons. Finally, larger whisker deflections evoked excitation spreading over the entire barrel field within approximately 50 msec before subsiding over the next approximately 250 msec. Thus the subthreshold cortical map representing a whisker deflection is dynamic on the millisecond time scale and strongly depends on stimulus strength. The sequential spatiotemporal activation of the excitatory neuronal network in L2/3 by a simple sensory stimulus can thus be accounted for primarily by the columnar restriction of L4 to L2/3 excitatory connections and the axonal field of barrel-related pyramids.