Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

Abstract

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.

Interdependence of primary and secondary somatosensory cortices for plasticity and texture discrimination learning

“…It may not be entirely surprising that S1 is required for such learning as the discrimination is performed by the whiskers (Pacchiarini et al, 2020) and the barrel cortex is the major recipient of the somatosensory projection from the whiskers via the brainstem and the thalamus (VPm). Indeed, these findings are in agreement with previous studies in rat showing that barrel cortex ablation prevents whisker-based texture discrimination (Guic-Robles et al, 1992) and while detection of an object per se does not appear to require S1, more complex discriminations do (Ryan et al, 2022). However, S2 also receives a somatosensory thalamic input via POm, which theoretically could have bypassed the VPm!S1 route to enable learning.…”

Cortical circuitry mediating interareal touch signal amplification

“…Given that the touch responses of MW neurons in vS2 contribute disproportionately to the vS1 projection, we next asked how vS2 touch activity contributes to iso-somatotopic touch responses in vS1. We ablated the vS2 touch patch using prolonged exposure to a femtosecond laser source 41 ( STAR Methods ), resulting in a focal, superficial vS2 lesion ( Figures 4A – 4C ). Before and after vS2 lesions, we imaged vS1 using a single three-plane subvolume spanning 180 mm in total depth ( Table S1 ).…”

“…This population carries a large proportion of the interareal touch signal in both directions, especially from vS2 to vS1, and its synchrony suggests that it is especially effective at influencing downstream targets 36 ( Figure 3 ). Lesioning 41 the subregion of either area that responded to touch by the spared whiskers resulted in a decline in touch response in the iso-somatotopic subregion of the other area, with whisker-specific vS1 lesions producing whisker-specific vS2 effects ( Figures 4 and 5 ). We therefore propose that intracolumnar feedforward processing from L4 to L2 in vS1 and vS2 broadens receptive fields, yielding a sparse population of broadly tuned neurons that then recurrently amplify the touch response across iso-somatotopic subregions of both areas.…”

“…Moreover, both thalamocortical and corticothalamic projections are often topographically organized, 55 – 57 providing a further putative recurrent loop between vS1 and vS2. Finally, although our lesions typically target superficial layers, 41 dendrites of many neurons with somata below L2/3 will be cut, and L2/3 input will be eliminated, so that nearly all neurons below the lesion site are likely to exhibit reduced touch responsiveness. It is thus likely that a substantial portion of the lesion effect is due to polysynaptic pathways, either within cortex or via thalamus.…”

“…This approach consistently yields lesions with a volume of 0.1–0.2 mm 3 , and when performed in animals expressing GCaMP6s, the radius of the post-lesion calcium response can be used to infer lesion extent. 41 In animals where intentionally large lesions were made ( Figure S9 ), we made five or more additional lesions surrounding the initial lesion using the same depth, power, and timing parameters.…”