Single-Cell Stimulation in Barrel Cortex Influences Psychophysical Detection Performance

A single whisker stimulus elicits action potentials in a sparse subset of neurons in somatosensory cortex. The precise contribution of these neurons to the animal's perception of a whisker stimulus is unknown. Here we show that single-cell stimulation in rat barrel cortex of both sexes influences the psychophysical detection of a near-threshold whisker stimulus in a cell type–dependent manner, without affecting false alarm rate. Counterintuitively, stimulation of single fast-spiking putative inhibitory neurons increased detection performance. Single-cell stimulation of putative excitatory neurons failed to change detection performance, except for a small subset of deep-layer neurons that were highly sensitive to whisker stimulation and that had an unexpectedly strong impact on detection performance. These findings indicate that the perceptual impact of excitatory barrel cortical neurons relates to their firing response to whisker stimulation and that strong activity in a single highly sensitive neuron in barrel cortex can already enhance sensory detection. Our data suggest that sensory detection is based on a decoding mechanism that lends a disproportionally large weight to interneurons and to deep-layer neurons showing a strong response to sensory stimulation.

SIGNIFICANCE STATEMENT Rat whisker somatosensory cortex contains a variety of neuronal cell types with distinct anatomical and physiological characteristics. How each of these different cell types contribute to the animal's perception of whisker stimuli is unknown. We explored this question by using a powerful electrophysiological stimulation technique that allowed us to target and stimulate single neurons with different sensory response types in whisker cortex. In awake, behaving animals, trained to detect whisker stimulation, only costimulation of single fast-spiking inhibitory neurons or single deep-layer excitatory neurons with strong responses to whisker stimulation enhanced detection performance. Our data demonstrate that single cortical neurons can have measurable impact on the detection of sensory stimuli and suggest a decoding mechanism based on select cell types.