Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex

The rodent primary somatosensory cortex is spontaneously active in the form of locally synchronous membrane depolarizations (UP states) separated by quiescent hyperpolarized periods (DOWN states) both under anesthesia and during quiet wakefulness. In vivo whole-cell recordings and tetrode unit recordings were combined with voltage-sensitive dye imaging to analyze the relationship of the activity of individual pyramidal neurons in layer 2/3 to the ensemble spatiotemporal dynamics of the spontaneous depolarizations. These were either brief and localized to an area of a barrel column or occurred as propagating waves dependent on local glutamatergic synaptic transmission in layer 2/3. Spontaneous activity inhibited the sensory responses evoked by whisker deflection, accounting almost entirely for the large trial-to-trial variability of sensory-evoked postsynaptic potentials and action potentials. Subthreshold sensory synaptic responses evoked while a cortical area was spontaneously depolarized were smaller, briefer and spatially more confined. Surprisingly, whisker deflections evoked fewer action potentials during the spontaneous depolarizations despite neurons being closer to threshold. The ongoing spontaneous activity thus regulates the amplitude and the time-dependent spread of the sensory response in layer 2/3 barrel cortex.

Facilitating sensory responses in developing mouse somatosensory barrel cortex

Carl Petersen, James Poulet

The sensory responses in the barrel cortex of mice aged postnatal day (P)7-P12 evoked by a single whisker deflection are smaller in amplitude and spread over a smaller area than those measured in P13-P21 mice. However, repetitive 10-Hz stimulation or paired pulse whisker stimulation in P7-P12 mice evoked facilitating sensory responses, contrasting with the depressing sensory responses observed in P13-P21 mice. This facilitation occurred during an interval ranging 300-1,000 ms after the first stimulus and was measured using whole cell recordings, voltage-sensitive dye imaging, and calcium-sensitive dye imaging. The facilitated responses were not only larger in amplitude but also propagated over a larger cortical area. The facilitation could be blocked by local application of pharmacological agents reducing cortical excitability. Local cortical microstimulation could substitute for the first whisker stimulus to produce a facilitated sensory response. The enhanced sensory responses evoked by repetitive sensory stimuli in P7-P12 mice may contribute to the activity-dependent specification of the developing cortical circuits. In addition, the facilitating sensory responses allow long integration times for sensory processing compatible with the slow behavior of mice during early postnatal development.

2007

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

Carl Petersen

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.

2003

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

Carl Petersen

2003