Independent representations of self-motion and object location in barrel cortex output.

During active tactile exploration, the dynamic patterns of touch are transduced to electrical signals and transformed by the brain into a mental representation of the object under investigation. This transformation from sensation to perception is thought to be a major function of the mammalian cortex. In primary somatosensory cortex (S1) of mice, layer 5 (L5) pyramidal neurons are major outputs to downstream areas that influence perception, decision-making, and motor control. We investigated self-motion and touch representations in L5 of S1 with juxtacellular loose-seal patch recordings of optogenetically identified excitatory neurons. We found that during rhythmic whisker movement, 54 of 115 active neurons (47%) represented self-motion. This population was significantly more modulated by whisker angle than by phase. Upon active touch, a distinct pattern of activity was evoked across L5, which represented the whisker angle at the time of touch. Object location was decodable with submillimeter precision from the touch-evoked spike counts of a randomly sampled handful of these neurons. These representations of whisker angle during self-motion and touch were independent, both in the selection of which neurons were active and in the angle-tuning preference of coactive neurons. Thus, the output of S1 transiently shifts from a representation of self-motion to an independent representation of explored object location during active touch.

Behavioral and Neural Bases of Tactile Shape Discrimination Learning in Head-Fixed Mice.

Tactile shape recognition requires the perception of object surface angles. We investigate how neural representations of object angles are constructed from sensory input and how they reorganize across learning. Head-fixed mice learned to discriminate object angles by active exploration with one whisker. Calcium imaging of layers 2-4 of the barrel cortex revealed maps of object-angle tuning before and after learning. Three-dimensional whisker tracking demonstrated that the sensory input components that best discriminate angles (vertical bending and slide distance) also have the greatest influence on object-angle tuning. Despite the high turnover in active ensemble membership across learning, the population distribution of object-angle tuning preferences remained stable. Angle tuning sharpened, but only in neurons that preferred trained angles. This was correlated with a selective increase in the influence of the most task-relevant sensory component on object-angle tuning. These results show how discrimination training enhances stimulus selectivity in the primary somatosensory cortex while maintaining perceptual stability.