Proceedings of The Physiological Society
Cardiff University (2009) Proc Physiol Soc 17, C12
Rapid, learning-induced inhibitory synaptogenesis in murine barrel field
S. Glazewski1, M. Jasinska2, E. Siucinska3, A. Cybulska-Klosowicz3, E. Pyza2, D. N. Furness1, M. Kossut3
1. School of Life Sciences, Keele University, Keele, United Kingdom. 2. Institute of Zoology, Jagiellonian University, Krakow, Poland. 3. The Nencki Institute, Warsaw, Poland.
The structure of neurones changes during development and in response to injury or alteration in sensory experience. Changes occur in the number, shape and dimensions of dendritic spines together with their synapses. However, precise data on these changes in response to learning are sparse. Here, after a period of habituation, mice were conditioned according to classical (Pavlovian) paradigm. A stroke of the selected whisker (CS) on one side of the snout was paired with a mild tail shock (UCS) (Siucinska & Kossut, 1996). We show using quantitative transmission electron microscopy (TEM) that a simple form of learning involving mystacial vibrissae in mice results in about 70% increase in the density of inhibitory synapses on spines of neurones located in layer IV barrels that represent the stimulated vibrissae (control, 0.27 SD ± 0.05 per μm3 versus conditioned, 0.47 ± SD 0.09 per μm3; ANOVA, p<0.001, F= 14.94, total df=27). The spines contain one asymmetrical (excitatory) and one symmetrical (inhibitory) synapse (double-synapse spines) and their density increases 3-fold due to learning with no apparent change in the density of asymmetrical synapses (control, 0.10 ± 0.03 versus conditioned, 0.29 ± 0.07 per μm3; ANOVA, p<0.001, F=18.95, total df=27). This effect seems to be specific for learning as pseudoconditioning (where the conditioned and unconditioned stimuli are delivered at random) does not lead to the enhancement of symmetrical synapses, but instead results in an up-regulation of asymmetrical synapses on spines (controls, 1.19 SD ± 0.15 per μm3 versus pseudoconditioned, 2.34 SD ± 0.62 per μm3; ANOVA, p<0.001, F=14.46 and total df=27). Symmetrical synapses of cells located in barrels receiving the conditioned stimulus show also a greater concentration of γ-amino-butyric acid (GABA) in their presynaptic terminals as measured with immunogold histochemistry under the TEM (control,12.31 gold particles per μm2 ± SE 3.59 versus conditioned, 27.06 gold particles per μm2 SE ± 4.83; Mann-Whitney, p<0.0001, 3 animals per group; control, 147 symmetrical terminals counted versus conditioned, 153 symmetrical terminals counted). These results indicate that the immediate effect of classical conditioning in the ‘conditioned’ barrels is rapid, pronounced and inhibitory.
Where applicable, experiments conform with Society ethical requirements