Cerebral cortex supports representations of the world in patterns of neural activity, used by the brain to make decisions and guide behavior. Past work has found diverse or limited changes in the primary sensory cortex in response to learning, suggesting the key computations might occur in downstream regions. Alternatively, sensory cortical changes may be central to learning. To study changes in sensory cortical representations, we trained mice to recognize entirely novel, non-sensory patterns of cortical activity in the primary visual cortex (V1) created by direct optogenetic stimulation. As animals learned to use these novel patterns, we found their detection abilities improved by an order of magnitude or more. The behavioral change was accompanied by large increases in V1 neural responses to fixed optogenetic input. Neural response amplification to novel optogenetic inputs had little effect on existing visual sensory responses. Amplification would seem to be desirable to improve decision-making in a detection task, and thus these data suggest adult cortical plasticity plays a significant role in improving the detection of novel sensory inputs during learning.
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.
Sensory cortical areas are often organized into topographic maps which represent the sensory epithelium. Individual areas are richly interconnected, in many cases via reciprocal projections that respect the topography of the underlying map. Because topographically matched cortical patches process the same stimulus, their interaction is likely central to many neural computations. 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.
Primary sensory cortex is a key locus of plasticity during learning. Exposure to novel stimuli often alters cortical activity, but isolating cortex-specific dynamics is challenging due to extensive pre-cortical processing. Here, we employ optical microstimulation of pyramidal neurons in layer (L) 2/3 of mouse primary vibrissal somatosensory cortex (vS1) to study cortical dynamics as mice learn to discriminate microstimulation intensity. Tracking activity over weeks using two-photon calcium imaging, we observe a rapid sparsification of the photoresponsive population, with the most responsive neurons exhibiting the largest declines in responsiveness. Following sparsification, the photoresponsive population attains a stable rate of neuronal turnover. At the same time, the photoresponsive population increasingly overlaps with populations encoding whisker movement and touch. Finally, we find that mice with larger declines in responsiveness learn the task more slowly than mice with smaller declines. Our results reveal that microstimulation-evoked cortical activity undergoes extensive reorganization during task learning and that the dynamics of this reorganization impact perception.
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