Lifelong impact of variations in maternal care on dendritic structure and function of cortical layer 2/3 pyramidal neurons in rat offspring

Abstract

Maternal licking and grooming (LG) exerts profound influence on hippocampal development and function in the offspring. However, little information is available on the effects of variations in maternal care on other brain regions. Here we examined the effects of variation in the frequency of maternal LG on morphological and electrophysiological properties of layer 2/3 pyramidal neurons in the somatosensory cortex in adult offspring. Compared to low LG offspring, high LG offspring displayed decreased dendritic complexity, reduced spine density and decreased amplitude of spontaneous postsynaptic currents. These changes were accompanied by higher levels of reelin expression in offspring of high LG mothers. Taken together, these findings suggest that differential amount of naturally-occurring variations in maternal LG is associated with enduring changes in dendritic morphology and synaptic function in layer 2/3 pyramidal neurons of the somatosensory cortex.

Figure 1. Maternal LG has a lifelong effect on dendritic complexity and total spine density in the cortex.

(A) Representative examples of reconstructed cortical layer 2/3 pyramidal neurons in the somatosensory cortex of male adult high and low LG rats. (B,C) Dendritic complexity index calculated for the apical (B) and basal (C) dendrites of layer 2/3 pyramidal neurons of high and low LG rats. (D) Representative images of Golgi-impregnated segments from apical and basal dendrites of layer 2/3 pyramidal neurons in the somatosensory cortex of male adult high and low LG rats. (E,F) Average total spine distribution per 20 µm on the apical (E) and basal (F) dendrites in high and low LG rats. (G,H) Average spine distribution per 20 µm for each spine subtype on the apical (G) and basal (H) dendrites of high and low LG rats. Data are expressed as the mean±SEM. Asterisks indicate significant differences (* p<0.05, ** p<0.01).

Figure 2. Maternal LG affects the amplitude of spontaneous postsynaptic currents in cortical layer 2/3 pyramidal neurons.

(A,B) Typical examples of evoked action potentials (A) and recordings of spontaneous postsynaptic currents (B) obtained from layer 2/3 pyramidal neurons in the somatosensory cortex of male adult high and low LG rats. (C,D) Normalized cumulative frequency (C) and cumulative amplitude (D) of spontaneous events recorded from layer 2/3 pyramidal neurons. The amplitude distribution of high LG rats is shifted leftwards as compared to low LG rats (p<0.01, Kolgomorov-Smirnov test), whereas the frequency distributions do not differ significantly.

Figure 3. Differential reelin levels in the cortex of adult high and low LG rats.

(A) Western blots immunoprobed for reelin with three bands at 450, 370 and 180 kDA corresponding to the full length and truncated reelin fragments in high and low LG rats. (B) Reelin immunoreactivity expressed as a ratio in optical density for reelin/ β actin for the accumulative reelin bands from high LG and low LG rats. Data are expressed as the mean±SEM. Asterisks indicate significant differences (* p<0.05).