Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation

Dev Neurobiol. 2008 Nov;68(13):1463-73. doi: 10.1002/dneu.20667.

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.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acoustic Stimulation / methods
  • Afferent Pathways / cytology*
  • Afferent Pathways / embryology*
  • Age Factors
  • Animals
  • Animals, Newborn
  • Auditory Perception / physiology*
  • Behavior, Animal / physiology*
  • Behavior, Animal / radiation effects
  • Brain Mapping
  • Chi-Square Distribution
  • Choice Behavior / physiology
  • Embryo, Nonmammalian
  • Immediate-Early Proteins / metabolism
  • Maternal Behavior / physiology
  • Photic Stimulation / methods
  • Quail / embryology
  • Reaction Time / physiology
  • Sensory Receptor Cells / metabolism
  • Visual Perception / physiology*
  • Vocalization, Animal / physiology

Substances

  • Immediate-Early Proteins