Sensory maps in layer (L) 2/3 of rodent cortex lack precise functional column boundaries, and instead exhibit locally heterogeneous (salt-and-pepper) tuning superimposed on smooth global topography. Could this organization be a byproduct of impoverished experience in laboratory housing? We compared whisker map somatotopy in L2/3 and L4 excitatory cells of somatosensory (S1) cortex in normally housed vs. tactile-enriched mice, using GCaMP6s imaging. Normally housed mice had a dispersed, salt-and-pepper whisker map in L2/3, but L4 was more topographically precise. Enrichment (P21 to P46-71) sharpened whisker tuning and decreased, but did not abolish, local tuning heterogeneity. In L2/3, enrichment strengthened and sharpened whisker point representations, and created functional boundaries of tuning similarity and noise correlations at column edges. Thus, enrichment drives emergence of functional columnar topography in S1, and reduces local tuning heterogeneity. These changes predict better touch detection by neural populations within each column.
Rodent sensory cortex contains salt-and-pepper maps of sensory features, whose structure is not fully known. Here we investigated the structure of the salt-and-pepper whisker somatotopic map among L2/3 pyramidal neurons in somatosensory cortex, in awake mice performing one-vs-all whisker discrimination. Neurons tuned for columnar (CW) and non-columnar (non-CW) whiskers were spatially intermixed, with co-tuned neurons forming local (20 µm) clusters. Whisker tuning was markedly unstable in expert mice, with 35-46% of pyramidal cells significantly shifting tuning over 5-18 days. Tuning instability was highly concentrated in non-CW tuned neurons, and thus was structured in the map. Instability of non-CW neurons was unchanged during chronic whisker paralysis and when mice discriminated individual whiskers, suggesting it is an inherent feature. Thus, L2/3 combines two distinct components: a stable columnar framework of CW-tuned cells that may promote spatial perceptual stability, plus an intermixed, non-columnar surround with highly unstable tuning.
That experience shapes sensory tuning in primary sensory cortex is well understood. But effective neural population codes depend on more than just sensory tuning. Recent population imaging and recording studies have characterized population codes in sensory cortex, and tracked how they change with sensory manipulations and training on perceptual learning tasks. These studies confirm sensory tuning changes, but also reveal other features of plasticity, including sensory gain modulation, restructuring of firing correlations, and differential routing of information to output pathways. Unexpectedly strong day-to-day variation exists in single-neuron sensory tuning, which stabilizes during learning. These are novel dimensions of plasticity in sensory cortex, which refine population codes during learning, but whose mechanisms are unknown.
The whisker map in rodent somatosensory cortex is well characterized under anesthesia, but its organization during awake sensation, when cortical coding can differ strongly, is unknown. Using a novel behavioral task, we measured whisker receptive fields and maps in awake mice with 2-photon calcium imaging in vivo. During a whisker-attentive task, layer 2/3 pyramidal neurons were sharply tuned, with cells tuned to different whiskers intermixed in each column. This salt-and-pepper organization consisted of small clusters of similarly-tuned neurons superimposed on a mean subcolumnar map. Parvalbumin interneurons had broader tuning, and were more homogeneously tuned to the columnar whisker. During a sound-attentive task, whisker tuning of pyramidal cells was less heterogeneous in each column, and firing correlations increased. Thus, behavioral demands modulate fine-scale map structure, and decorrelate the whisker map during whisker-attentive behavior.
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