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Peron, S. P.

Publications and source records attributed to Peron, S. P..

8 recordsLinked to original sources

Representational drift in barrel cortex is receptive field dependent

Cortical populations often exhibit changes in activity even when behavior is stable. How behavioral stability is maintained in the face of such representational drift remains unclear. One possibility is that some neurons are stable despite broader instability. We examine whisker touch responses in superficial layers of primary vibrissal somatosensory cortex (vS1) over several weeks in mice stably performing an object detection task with two whiskers. While the number of touch neurons remained constant, individual neurons changed with time. Touch-responsive neurons with broad receptive fields were more stable than narrowly tuned neurons. Transitions between functional types were non-random: before becoming broadly tuned neurons, unresponsive neurons first pass through a period of narrower tuning. Broadly tuned neurons with higher pairwise correlations to other touch neurons were more stable than neurons with lower correlations. Thus, a small population of broadly tuned and synchronously active touch neurons exhibit elevated stability and may be particularly important for downstream readout.

neuroscience↗

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.

neuroscience↗

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.

neuroscience↗

Microstimulation of sensory cortex engages natural sensory representations

Cortical activity patterns occupy a small subset of possible network states. If this is due to intrinsic network properties, microstimulation of cortex should evoke activity patterns resembling those observed during natural sensory input. Here, we use optical microstimulation of virally transfected layer 2/3 pyramidal neurons in mouse primary vibrissal somatosensory cortex to compare artificially evoked activity with natural activity evoked by whisker touch and movement ( whisking). We find that photostimulation engages touch but not whisking responsive neurons more than expected by chance. Neurons that respond to photostimulation and touch or to touch alone exhibit higher spontaneous pairwise correlations than purely photoresponsive neurons. Exposure to several days of simultaneous touch and optogenetic stimulation raises both overlap and spontaneous activity correlations among touch and photoresponsive neurons. We thus find that cortical microstimulation engages existing cortical representations and that repeated co-presentation of natural and artificial stimulation enhances this effect.

neuroscience↗

Columnar scale lesions in barrel cortex degrade tactile discrimination but not detection

Primary sensory cortices typically display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Because traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), barrels with a radius of [~]150 m 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 an average volume of [~]2 barrels. These columnar scale lesions impair performance on object location discrimination tasks without disrupting vibrissal kinematics. Animals with degraded discrimination performance can immediately perform a detection task with high accuracy. Animals trained de novo on both simple and complex detection tasks showed no behavioral deficits following columnar scale lesions. Thus, vS1 barrels are necessary for performing object location discrimination but not simple or complex object detection behaviors.

neuroscience↗

Sensory cortical dynamics during optical microstimulation training

Sensory cortical representations can be highly dynamic, raising the question of how representational stability impacts perception. We used volumetric two-photon calcium imaging to track neural activity as mice learned an optical microstimulation task. Mice were required to report the number of photostimulation pulses delivered to opsin-expressing neurons in layer 2/3 of primary vibrissal somatosensory cortex. We found that the amount of photostimulus-evoked activity could predict animal choice. Over the course of training, this photostimulus-evoked activity rapidly declined, particularly among highly photoresponsive neurons. Population activity levels across training were similar between animals that learned and those that did not. However, the photoresponsive population exhibited turnover both within and across behavioral sessions that was elevated among animals that failed to learn. Animals that failed to learn also exhibited a faster deterioration in stimulus decoding. Our results show that the rate at which sensory cortical representations change constrains learning and impacts behavior.

neuroscience↗

Transformation of Primary Sensory Cortical Representations from Layer 4 to Layer 2

Sensory input arrives from thalamus in cortical layer (L) 4, from which it flows predominantly to superficial layers, so that L4 to L2 constitutes one of the earliest cortical feedforward networks. Despite extensive study, the transformation performed by this network remains poorly understood. We use two-photon calcium imaging in L2-4 of primary vibrissal somatosensory cortex (vS1) to record neural activity as mice perform an object localization task with two whiskers. We find that touch responses sparsen but become more reliable from L4 to L2, with superficial neurons responding to a broader range of touches. Decoding of sensory features either improves from L4 to L2 or remains unchanged. Pairwise correlations increase superficially, with L2/3 containing ensembles of mostly broadly tuned neurons responding robustly to touch. Thus, from L4 to L2, cortex transitions from a dense probabilistic code to a sparse and robust ensemble-based code that improves stimulus decoding, facilitating perception.

neuroscience↗

Recurrent interactions in local cortical circuits

The majority of cortical synapses are local and excitatory. Local recurrent circuits could implement amplification, allowing for pattern completion and other computations1. Cortical circuits contain subnetworks, consisting of neurons with similar receptive fields and elevated connectivity relative to the network average2,3. Understanding the computations performed by these subnetworks during behavior has been hampered by the fact that cortical neurons encoding different types of information are spatially intermingled and distributed over large brain volumes 4,5. We used computational modeling, optical recordings and manipulations to probe the function of recurrent coupling in layer (L) 2/3 of the somatosensory cortex during tactile discrimination. A model of L2/3 dynamics revealed that recurrent excitation enhances sensory signals via amplification, but only for subnetwork with elevated connectivity. Networks with high amplification were sensitive to damage: loss of a few subnetwork members degraded stimulus encoding. We tested this prediction experimentally by mapping neuronal selectivity5 and photoablating6,7 neurons with specific selectivity. In L2/3 of the somatosensory cortex, ablating a small proportion (10-20, < 5 % of the total) of neurons representing touch dramatically reduced responses in the spared touch representation, but not other representations. Network models further predicted that degradation following ablation should be greatest among spared neurons with stimulus responses that were most similar to the ablated population. Consistent with this prediction, ablations most strongly impacted neurons with selectivity similar to the ablated population. Our data shows that recurrence among cortical neurons with similar selectivity can drive input-specific amplification during behavior.

neuroscience↗