Sensory deprivation differentially impacts the dendritic development of pyramidal versus non-pyramidal neurons in layer 6 of mouse barrel cortex

Abstract

Early postnatal sensory experience can have profound impacts on the structure and function of cortical circuits affecting behavior. Using the mouse whisker-to-barrel system we chronically deprived animals of normal sensory experience by bilaterally trimming their whiskers every other day from birth for the first postnatal month. Brain tissue was then processed for Golgi staining and neurons in layer 6 of barrel cortex were reconstructed in three dimensions. Dendritic and somatic parameters were compared between sensory-deprived and normal sensory experience groups. Results demonstrated that layer 6 non-pyramidal neurons in the chronically deprived group showed an expansion of their dendritic arbors. The pyramidal cells responded to sensory deprivation with increased somatic size and basilar dendritic arborization but overall decreased apical dendritic parameters. In sum, sensory deprivation impacted on the neuronal architecture of pyramidal and non-pyramidal neurons in layer 6, which may provide a substrate for observed physiological and behavioral changes resulting from whisker trimming.

Fig. 1

Golgi-stained section of the barrel cortex. a Low magnification image (×4) illustrating barrel cortex and its six distinct layers bounded by pia and the white matter. The white box highlights the region magnified in b; Scale bar 250 µm. b Higher magnification (×10) highlighting the morphologies of layer 6 (L6) neurons. Scale bar 250 µm. c Higher magnification (×20) of a single pyramidal neuron located in L6. Scale bar 50 µm. d High magnification (×100) of the region in white in c. Please note the presence of dendritic spines, demonstrating the entirety of the neuronal labeling. Scale bar 50 µm. e High magnification (×100) of the region in black in f. Please note the relative absence of dendritic spines. Scale bar 25 µm. f ×20 magnification of a typical labeled non-pyramidal neuron located in L6. Scale bar 25 µm

Fig. 2

Representative reconstructed neurons. a, b Reconstructed L6 pyramidal neurons in the control P30 and sensory-deprived P30, respectively. c, d Reconstructed L6 non-pyramidal neurons in the control P30 and sensory-deprived P30, respectively. All scale bars 50 µm

Fig. 3

Effect of chronic sensory deprivation on dendritic parameters of L6 non-pyramidal neurons. a Dendritic morphometric variables in control versus sensory-deprived animals. Overall, dendritic parameters increased dramatically (with the exception of dendritic quantity) following chronic sensory deprivation in developing animals; means and one standard error of the mean are plotted. b Mean number of dendritic intersections between 10-µm concentric spheres in control versus sensory-deprived mice. Increased number of dendritic intersections in sensory-deprived relative to control mice was distributed mostly within the first 90 µm, suggesting that the effect was relatively localized. c Mean number of dendritic lengths between 10-µm concentric spheres in control versus sensory-deprived mice. Similar to mean number of dendritic intersections, the increased dendritic length in sensory-deprived relative to control mice were distributed mostly within the first 110 µm of the dendrite, indicating that the effect was localized. Error bars indicate standard error of the mean (SEM). Asterisks indicates statistical significance of post hoc tests (Tukey HSD) at individual levels (p < 0.05)

Fig. 4

Effect of chronic sensory deprivation on apical dendritic parameters of L6 pyramidal neurons. a Apical dendritic morphometric variables in control versus sensory-deprived animals. Apical dendritic parameters showed significant decrease (with the exception of dendritic quantity and number of bi/trifurcations) following chronic sensory deprivation in developing animals; means and one standard error of the mean are plotted. b Mean number of apical dendritic intersections between 10-µm concentric spheres in control versus sensory-deprived mice. The decreased number of dendritic intersections in sensory-deprived relative to control mice was distributed from 120 to 180 µm from the center of the soma, suggesting that the effect was relatively distal and might be outside of L6. c Mean number of apical dendritic lengths between 10-µm concentric spheres in control versus sensory-deprived mice. Similar to mean number of apical dendritic intersections, the decreased apical dendritic length in sensory-deprived relative to control mice was distributed mostly from 90 to 190 µm away from the soma. Error bars indicate standard error of the mean (SEM). Asterisks indicate statistical significance of post hoc tests (Fisher LSD) at individual levels (p <0.05)

Fig. 5

Effect of chronic sensory deprivation on basilar dendritic parameters of L6 pyramidal neurons. a Basilar dendritic morphometric variables in control versus sensory-deprived animals. Basilar dendritic parameters showed an overall trend to increase significantly (including dendritic nodes, dendritic ends, and dendritic length) following chronic sensory deprivation in developing animals; means and one standard error of the mean are plotted. b Mean number of basilar dendritic intersections between 10-µm concentric spheres in control versus sensory-deprived mice. The increased number of dendritic intersections in sensory-deprived relative to control mice was distributed from 20 to 50 µm away from the center of the soma, suggesting that the effect is relatively localized. c Mean number of basilar dendritic lengths between 10-µm concentric spheres in control versus sensory-deprived mice. Similar to mean number of basilar dendritic intersections, the decreased basilar dendritic length in sensory-deprived relative to control animals was distributed mostly from 30 to 60 µm away from the soma, indicating the localized effect of sensory deprivation on the development of basilar dendrites. Error bars indicate standard error of the mean (SEM). Asterisks indicate statistical significance of post hoc tests (Fisher LSD) at individual levels (p < 0.05)