Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input

Of all sensory areas, barrel cortex is among the best understood in terms of circuitry, yet least understood in terms of sensory function. We combined intracellular recording in rats with a novel multi-directional multi-whisker stimulator system to estimate receptive fields by reverse correlation of stimuli to synaptic inputs. Spatiotemporal receptive fields were identified orders of magnitude faster than by conventional spike-based approaches, even for neurons with little spiking activity. Given a suitable stimulus representation, a linear model captured the stimulus-response relationship for all neurons with surprisingly high accuracy. In contrast to conventional single-whisker stimuli, complex stimuli revealed dramatically sharpened receptive fields, largely due to adaptation. This phenomenon allowed the surround to facilitate rather than suppress responses to the principal whisker. Optimized stimuli enhanced firing in layers 4-6 but not 2/3, which remained sparsely active. Surround facilitation through adaptation may be required for discriminating complex shapes and textures during natural sensing.