Perhaps more than any other time in her life, the female rat must exhibit efficient responses as she balances the challenges of caring for her offspring with the continued need to meet her own metabolic demands. In addition to the more traditionally viewed maternal behaviors including nursing, retrieving, and grooming her pups, successful maternal rats must engage in efficient foraging responses in order to minimize time spent off the nest at a time when her offspring are vulnerable to predation. Indeed, our laboratory* has found that both maternal (primiparous and multiparous) and pup-sensitized females exhibit enhanced learning ability in a foraging task (Kinsley et al., 1999). Longitudinal explorations confirmed the long-lasting nature of these effects. Reductions in anxiety-like behaviors have also been observed in maternal rats; specifically, primiparous and multiparous animals are more curious and exploratory in the elevated plus maze, an effect that also appears to persist throughout the maternal rat’s life (Love et al., 2005; Kinsley & Lambert, 2006). After finding that the maternal rats were also successful in more complex and ecologically relevant foraging tasks including social competition and hunting live crickets, we are currently focusing on the cognitive strategy of attention set-shifting. Results suggest that maternal rats, especially the multiparous animals, demonstrate faster latencies and fewer errors in this task, requiring them to focus their attention on salient cues (e.g., a specific odor) while ignoring distracting cues (e.g., digging medium) in order to more quickly obtain the food reward. Neurobiological examinations have also been conducted to determine the specific mechanisms underlying these maternal-induced behavioral alterations. During pregnancy, we have found increased dendritic spines in the CA1 area of the hippocampus and increased hippocampal glial fibrillary acidic protein (GFAP) immunoreactivity (continuing through lactation). Although we did not find alterations in CA1 morphology in old-age maternal rats in the longitudinal studies, we found fewer deposits of amyloid precursor protein (a hallmark of Alzheimer’s Disease) in older rats with maternal experience (Gatewood et al., 2005). Finally, our most recent work suggests that maternal rats exhibiting enhanced performance in the attention tasks have more nestin-immunoreactivity (Nestin is a class IV intermediate filament protein typically used as a marker for uncommitted progenitor cells but has more recently been found in mature neurons–perhaps indicating cytoskeletal plasticity in these nestin-expressing neurons; Rao et al., 2004) in the CA1 and CA3 areas of the hippocampus, indicating structural changes in these brain areas critical for spatial learning and problem solving. Related to the enhanced boldness observed in maternal animals, less c-fos immunoreactivity was observed in the CA3 area of the hippocampus and basolateral amygdala (both known for their involvement in stress responses). Further, a histological assessment of wild-caught pregnant and lactating rats revealed larger neuronal cell bodies in the basolateral amygdala than observed in the nonreproductive animals, perhaps related to maternal defensive responses. These histological data corroborate the aforementioned behavioral findings, suggesting that the maternal rat’s brain is altered in ways leading to enhanced efficiency in foraging and problem solving tasks, as well as reductions in metabolically costly anxiety/stress responses. In addition to our explorations of maternal rats, we are currently exploring the effects of parental experience on the brain by examining paternal behavior in the monogamous and bi-parental California Deer Mouse (Peromyscus californicus). Thus far, the paternal deer mice exhibit enhanced foraging and diminished anxiety in exploratory tasks as observed in the maternal rats. When exposed to pups restrained in a small enclosure, mice with paternal experience exhibited greater c-fos activation in the CA1 and prefrontal cortical areas than their nonpaternal counterparts. These initial findings suggest that paternal, as well as maternal, behavior contributes to significant neurobiological and behavioral alterations leading to adaptive responses for successful nurturing of offspring. * This research was conducted in collaboration with Dr. Craig Kinsley and his students at the University of Richmond, Richmond, VA USA. Acknowledgements: The current research was supported by NIH (1-R15-HD37578-01) and the Psychology Departments at Randolph-Macon College and the University of Richmond.Reference 1 : Gatewood, J.D. et al. (2005). Brain Res Bull 66, 91-98.Reference 2 : Love, G., et al. (2005). Behav Neurosci 119, 1084-1096Reference 3 : Kinsley, C.H., et al. (1999). Nature 402, 137.Reference 4 : Kinsley, C.H., & Lambert, K.G. (2006). Sci Am 294, 72-79.Reference 5 : Rao, A.J. et al. (2004). Society for Neuroscience Abstracts #719.17.
University of Edinburgh (2007) Proc Physiol Soc 6, SA11
Research Symposium: Maternal-Induced Neurobiological and Behavioral Plasticity
K. Lambert1
1. Psychology, Randolph-Macon College, Ashland, Virginia, United Kingdom.
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Where applicable, experiments conform with Society ethical requirements.