Cortical circuitry mediating interareal touch signal amplification.

Sensory cortical areas are organized into topographic maps representing the sensory epithelium. Interareal projections typically connect topographically matched subregions across areas. Because matched subregions process the same stimulus, their interaction is central to many computations. Here, we ask how topographically matched subregions of primary and secondary vibrissal somatosensory cortices (vS1 and vS2) interact during active touch. Volumetric calcium imaging in mice palpating an object with two whiskers revealed a sparse population of highly responsive, broadly tuned touch neurons especially pronounced in layer 2 of both areas. These rare neurons exhibited elevated synchrony and carried most touch-evoked activity in both directions. Lesioning the subregion of either area responding to the spared whiskers degraded touch responses in the unlesioned area, with whisker-specific vS1 lesions degrading whisker-specific vS2 touch responses. Thus, a sparse population of broadly tuned touch neurons dominates vS1-vS2 communication in both directions, and topographically matched vS1 and vS2 subregions recurrently amplify whisker touch activity.

Sparse and distributed cortical populations mediate sensorimotor integration.

Touch information is central to sensorimotor integration, yet little is known about how cortical touch and movement representations interact. Touch- and movement-related activity is present in both somatosensory and motor cortices, making both candidate sites for touch-motor interactions. We studied touch-motor interactions in layer 2/3 of the primary vibrissal somatosensory and motor cortices of behaving mice. Volumetric two-photon calcium imaging revealed robust responses to whisker touch, whisking, and licking in both areas. Touch activity was dominated by a sparse population of broadly tuned neurons responsive to multiple whiskers that exhibited longitudinal stability and disproportionately influenced interareal communication. Movement representations were similarly dominated by sparse, stable, reciprocally projecting populations. In both areas, many broadly tuned touch cells also produced robust licking or whisking responses. These touch-licking and touch-whisking neurons showed distinct dynamics suggestive of specific roles in shaping movement. Cortical touch-motor interactions are thus mediated by specialized populations of highly responsive, broadly tuned neurons.

Cortical circuitry mediating inter-areal touch signal amplification.

Sensory cortical areas are often organized into topographic maps which represent the sensory epithelium1,2. Individual areas are richly interconnected3, in many cases via reciprocal projections that respect the topography of the underlying map4,5. Because topographically matched cortical patches process the same stimulus, their interaction is likely central to many neural computations6-10. Here, we ask how topographically matched subregions of primary and secondary vibrissal somatosensory cortices (vS1 and vS2) interact during whisker touch. In the mouse, whisker touch-responsive neurons are topographically organized in both vS1 and vS2. Both areas receive thalamic touch input and are topographically interconnected4. Volumetric calcium imaging in mice actively palpating an object with two whiskers revealed a sparse population of highly active, broadly tuned touch neurons responsive to both whiskers. These neurons were especially pronounced in superficial layer 2 in both areas. Despite their rarity, these neurons served as the main conduits of touch-evoked activity between vS1 and vS2 and exhibited elevated synchrony. Focal lesions of the whisker touch-responsive region in vS1 or vS2 degraded touch responses in the unlesioned area, with whisker-specific vS1 lesions degrading whisker-specific vS2 touch responses. Thus, a sparse and superficial population of broadly tuned touch neurons recurrently amplifies touch responses across vS1 and vS2.

Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance.

Primary sensory cortices display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), and few studies track recovery following loss-of-function perturbations. Consequently, the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), "barrels" with a radius of ∼150 µm receive input predominantly from a single whisker, partitioning vS1 into a topographic map of well defined columns. Here, we train animals implanted with a cranial window over vS1 to perform single-whisker perceptual tasks. We then use high-power laser exposure centered on the barrel representing the spared whisker to produce lesions with a typical volume of one to two barrels. These columnar-scale lesions impair performance in an object location discrimination task for multiple days without disrupting vibrissal kinematics. Animals with degraded location discrimination performance can immediately perform a whisker touch detection task with high accuracy. Animals trained de novo on both simple and complex whisker touch detection tasks showed no permanent behavioral deficits following columnar-scale lesions. Thus, columnar-scale lesions permanently degrade performance in object location discrimination tasks.