Individual differences in cortical connections of somatosensory cortex are associated with parental rearing style in prairie voles (Microtus ochrogaster)

Abstract

Early life sensory experiences have a profound effect on brain organization, connectivity and subsequent behavior. In most mammals, the earliest sensory inputs are delivered to the developing brain through tactile contact with the parents, especially the mother. Prairie voles (Microtus ochrogaster) are monogamous and, like humans, are biparental. Within the normal prairie vole population, both the type and amount of interactions, particularly tactile contact, that parents have with their offspring varies. The question is whether these early and pervasive differences in tactile stimulation and social experience between parent and offspring are manifest in differences in cortical organization and connectivity. To address this question we examined the cortical and callosal connections of the primary somatosensory area (S1) in high contact (HC) and low contact (LC) offspring using neuroanatomical tracing techniques. Injection sites within S1 were matched so that direct comparisons between these two groups could be made. We observed several important differences between these groups. The first was that HC offspring had a greater density of intrinsic connections within S1 compared to LC offspring. The HC offspring had a more restricted pattern of ipsilateral connections while LC offspring had dense connections with areas of parietal and frontal cortex that were more widespread. Finally, LC offspring had a broader distribution of callosal connections than HC offspring and a significantly higher percentage of callosal labeled neurons. To date, this is the first study that examines individual differences in cortical connections and suggests that they may be related to natural differences in parental rearing styles associated with tactile contact.

Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species

“…These differences in somatosensory connectivity produced by relatively subtle variation in early care point toward a different approach to tactile information processing in high contact and low contact offspring. The diffuse patterns of connections of low contact offspring may indicate an enhanced ability to integrate multimodal sensory information (Seelke et al, 2016). These results show that variation in parental behavior is associated with individual differences in cortical connectivity and may provide yet another pathway, in addition to differences in neuropeptide systems, for parental care to modulate later behavior in offspring via central mechanisms.…”

“…Neuroanatomical tracer injections into the primary somatosensory cortex (S1) show greater amounts of connectivity in S1 both contra-and ipsilateral from the injection site in high contact offspring, while low contact offspring have a greater number of connections in neighboring regions including the motor cortex and secondary somatosensory area/parietal ventral area, and nearly three times the total number of labeled cells contralaterally compared with high contact offspring (Seelke et al, 2016). These differences in somatosensory connectivity produced by relatively subtle variation in early care point toward a different approach to tactile information processing in high contact and low contact offspring.…”

Hypergravity within a critical period impacts on the maturation of somatosensory cortical maps and their potential for use-dependent plasticity in the adult

“…J Neurophysiol 115: 2740 -2760, 2016. First published February 17, 2016 doi:10.1152/jn.00900.2015.-We investigated experience-dependent plasticity of somatosensory maps in rat S1 cortex during early development.…”

“…By contrast, whisker trimming does not affect barrel-pattern formation (Fox 1992;Henderson et al 1992;Rema et al 2003;Simons and Land 1987) but impairs the neurophysiological properties of cortical neurons (Fox 1992;Rema et al 2003;Shoykhet et al 2005;Simons and Land 1987;Stern et al 2001) as well as whisker discrimination (Carvell and Simons 1996). Surprisingly, few studies have investigated the maturation of body somatotopic maps in the S1 cortex (Armstrong-James 1975;McCandlish et al 1993;Seelke et al 2012), and little is known about the experience-dependent plasticity of neural circuits underlying the postnatal development of these somatosensory maps.…”

Contralateral targeting of the corpus callosum

“…Interestingly, it was recently shown that offspring from naturally variable parental rearing styles in prairie voles (high contact and low contact) show differences in S1 connections, including a broader distribution and higher number of callosal connections in low contact offspring than in high contact offspring (Seelke et al, 2016). Similarly, developmental contingencies that animals face in their natural environment are known to shape the brain, resulting in a diversity of connections within and between the cortical hemispheres (Krubitzer et al, 2011).…”