A growing body of evidence highlights the impact of the early social environment for the adequate development of brain and behavior in animals and humans. Disturbances of this environment were found to be both maladaptive and adaptive to emotional and cognitive function. Using the semi-precocial, biparental rodent Octodon degus, we aimed to examine (i) the impact of age (juvenile/adult), sex (male/female), and (ii) "motivation" to solve the task (by applying increasing foot-shock-intensities) on two-way active avoidance (TWA) learning in socially reared degus, and (iii) whether early life stress inoculation by 1h daily parental separation during the first three weeks of life has maladaptive or adaptive consequences on cognitive function as measured by TWA learning. Our results showed that (i) juvenile degus, unlike altricial rats of the same age, can successfully learn the TWA task comparable to adults, and (ii) that learning performance improves with increasing "task motivation", irrespective of age and sex. Furthermore, we revealed that (iii) stress inoculation improves avoidance learning, particularly in juvenile males, quantitatively and qualitatively depending on "task motivation". In conclusion, the present study describes for the first time associative learning in O. degus and its modulation by early life stress experience as an animal model to study the underlying mechanisms of learning and memory in the stressed and unstressed brain. Although, stress is commonly viewed as being maladaptive, our data indicate that early life stress inoculation triggers developmental cascades of adaptive functioning, which may improve cognitive and emotional processing of stressors later in life.

A growing body of evidence supports the hypothesis that juvenile cognitive training shapes neural networks and behavior, and thereby determines the adult´s capacity for learning and memory. In particular, we have shown that infant rats, even though they do not develop an active avoidance strategy in a two-way active avoidance task, show as adults accelerated learning in the same learning task. This indicates that a memory trace was formed in the infant rats, which most likely is recruited during adult training. To identify the learning conditions, which are essential prerequisites to form this memory trace in infancy or adolescence, we investigated the critical impact of: (i) age, (ii) CS–UCS contingency, and (iii) pre-training intensity on this facilitating effect. We observed: (i) an age-dependent improvement of avoidance learning, (ii) that the beneficial impact of infant or adolescent pre-training on adult learning increases with the age at pre-training, (iii) that CS–UCS contingency during infant pre-training was most efficient to accelerate adult learning, (iv) that pre-training intensity (i.e. number of pre-training trials) was positively correlated with the pre-training induced acceleration of adult learning, and (v) that infant rats, compared to adolescent rats, need a higher training intensity to show learning improvement as adults. These results indicate that infant rats develop a goal-oriented escape strategy, which during adult training is replaced by an avoidance strategy, facilitated by the recruitment of the CS–UCS association, which has been learned during infant training. Based on these results the future challenge will be to identify the specific contribution of prefronto-limbic circuits in infant and adult learning in relation to their functional maturation.

Similar to maternal care, paternal care is a source of neonatal sensory stimulation, which in primates and rodents has been shown to be essential for developing structure and function of sensory cortices. The aim of our study in the biparental rodent Octodon degus was to assess the impact of paternal deprivation on dendritic and synaptic development in the somatosensory cortex. We (i) quantified the amount of paternal care in relation to total parental investment and (ii) compared dendritic and synaptic development of pyramidal neurons in the somatosensory cortex of animals raised by a single mother or by both parents. On the behavioral level we show that paternal care comprises 37% of total parent-offspring interactions, and that the somatosensory stimulation provided by the fathers primarily consists of huddling, licking/grooming, and playing. On the morphological level we found that, compared with offspring raised by both parents (mother and father), the father-deprived animals displayed significantly reduced spine numbers on the basal dendrites of pyramidal neurons. Furthermore, paternal deprivation induces hemispheric asymmetry of the dendritic morphology of somatosensory pyramidal neurons. Father-deprived animals show shorter and less complex basal dendrites in the left somatosensory cortex compared with the right hemisphere. These findings indicate that paternal deprivation results in delayed or retarded dendritic and synaptic development of somatosensory circuits.

Evidence is accumulating that early emotional experience interferes with the development of the limbic system, which is involved in perception and regulation of emotional behaviors as well as in learning and memory formation. Limbic brain regions, as well as hypothalamic regions and other, nonlimbic areas contain specific neuron subpopulations, which express and release corticotropin releasing factor (CRF). Since these neurons serve to connect limbic function to endocrine, stress‐related responses, we proposed that stressful experience during early postnatal brain development should interfere with the development of CRF‐containing neurons, particularly in brain regions essential for emotional regulation. Applying neonatal separation stress (daily 1 h separation from the parents and litter mates) as stressor, the number of immunocytochemically identified CRF‐expressing neurons/fibers was quantified in the amygdala, hippocampus, paraventricular nucleus of the hypothalamus, piriform cortex, and the somatosensory cortex of 3‐week‐old stressed and nonstressed Octodon degus , a semi‐precocial rodent. Compared to controls neonatally stressed animals showed significantly lower levels of CRF‐positive fibers (−60%) in the central amygdala, significantly less CRF‐positive neurons in the dentate gyrus (−28%) and the CA1 region (−29%) and significantly lower CRF cell densities in the somatosensory cortex (−26%). On the other hand, we found significantly higher numbers of CRF‐immunoreactive neurons in the basolateral amygdaloid complex (+192%) of stressed animals compared to nonstressed controls. No differences in CRF‐immunoreactive cell densities were detected in the other regions. Additional behavioral analysis revealed significantly elevated exploratory behavior (+34%) in stressed animals compared to controls, which might indicate reduced anxiety in the stressed animals. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2007

A quantitative anatomical study in the rodent anterior cingulate and somatosensory cortex, hippocampus, and lateral amygdala revealed region-, cell-, and dendrite-specific changes of spine densities in 3-week-old Octodon degus after repeated parental separation. In parentally separated animals significantly higher spine densities were found on the apical and basal dendrites of the cingulate cortex (up to 143% on apical and 138% on basal dendrite). Branching order analysis revealed that this effect is seen on all segments of the apical dendrite, whereas on the basal dendrites significantly higher spine densities were seen only on the outer branches (third to fifth dendritic segments). Increased spine densities were also observed on the hippocampal CA1 pyramidal neurons (up to 109% on the distal apical segments and up to 106% on the basal segment) compared with the control group. In contrast, significantly reduced spine densities were observed on the granule cell dendrites in the dentate gyrus (down to 92%) and on the apical dendrites in the medial nucleus of the amygdala (down to 95%). No significant changes of spine densities were seen in the somatosensory cortex (except for an increase in the proximal apical segments) and in the lateral nucleus of the dorsal amygdala (except for an increase in the proximal basal dendritic segments). These results demonstrate that repeated stressful emotional experience alters the balance of presumably excitatory synaptic inputs of pyramidal neurons in the limbic system. Such experience-induced modulations of limbic circuits may determine psychosocial and cognitive capacities during later life.