Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation

Abstract

Embryonic vision is generated and maintained by spontaneous neuronal activation patterns, yet extrinsic stimulation also sculpts sensory development. Because the sensory and motor systems are interconnected in embryogenesis, how extrinsic sensory activation guides multimodal differentiation is an important topic. Further, it is unknown whether extrinsic stimulation experienced near sensory sensitivity onset contributes to persistent brain changes, ultimately affecting postnatal behavior. To determine the effects of extrinsic stimulation on multimodal development, we delivered auditory stimulation to bobwhite quail groups during early, middle, or late embryogenesis, and then tested postnatal behavioral responsiveness to auditory or visual cues. Auditory preference tendencies were more consistently toward the conspecific stimulus for animals stimulated during late embryogenesis. Groups stimulated during middle or late embryogenesis showed altered postnatal species-typical visual responsiveness, demonstrating a persistent multimodal effect. We also examined whether auditory-related brain regions are receptive to extrinsic input during middle embryogenesis by measuring postnatal cellular activation. Stimulated birds showed a greater number of ZENK-immunopositive cells per unit volume of brain tissue in deep optic tectum, a midbrain region strongly implicated in multimodal function. We observed similar results in the medial and caudomedial nidopallia in the telencephalon. There were no ZENK differences between groups in inferior colliculus or in caudolateral nidopallium, avian analog to prefrontal cortex. To our knowledge, these are the first results linking extrinsic stimulation delivered so early in embryogenesis to changes in postnatal multimodal behavior and cellular activation. The potential role of competitive interactions between the sensory and motor systems is discussed.

Weak functional connectivity in the human fetal brain prior to preterm birth

“…Potential efficacy of prenatal neurobehavioral therapy is supported by growing evidence from non-human animals and from humans that learning occurs prior to birth. Markham and colleagues have demonstrated that birds learn about the calls of conspecifics while still in the egg, and that this embryonic programming alters neural cellular activation after birth and also characteristics of later vocalizations69. A landmark study by Partanen and colleagues presented evidence of experienced-based neuroplasticity in human fetuses .…”

The Integrated Development of Sensory Organization

“…For example, Markham, Shimizu, and Lickliter [79] presented augmented amounts of auditory stimulation to bobwhite quail embryos during early, middle, or late prenatal development and then tested postnatal responsiveness to species typical auditory and visual cues. Embyos receiving auditory stimulation during middle or late stages of prenatal development showed altered postnatal visual responsiveness when compared to controls.…”

The Cost and Benefit of Juvenile Training on Adult Perceptual Skill

“…The loss of early auditory experience perturbs normal perceptual maturation in young animals, including children (Gottlieb, 1975; Kerr et al, 1979; Halliday and Bishop, 2005; Kidd et al, 2002; Clements and Kelly, 1978; Knudsen et al, 1984; Kelly et al, 1987; Moore et al, 1999; Parsons et al, 1999). Similarly, chronic exposure to sound during development can disrupt normal perceptual sensitivity (Gottlieb, 1991; Han et al, 2007; Zhang et al, 2008; Markham et al, 2008). These findings are consistent with an even larger literature showing that neural coding, which often serves as a proxy for behavior, can be impacted by similar manipulations (for reviews, see Keuroghlian and Knudsen, 2007; Sanes and Bao, 2009)…”