Motility in the chick embryo in the absence of sensory input

Abstract

The following experiment was designed to test the role of sensory input in the motility of the chick embryo: Complete deafferentation of the leg level was accomplished i n 2-day embryos by extirpation of the dorsal half of the lumbar spinal cord including the precursor cells of spinal ganglia; and simultaneous extirpation of the entire spinal cord i n the thoracic level to exclude sensory input from more rostra1 levels. In control embryos, only the thoracic gap was made. The embryos were reared to eight and one-half, 11, 13, 15 and 17 days, respectively, and manual recordings were made of the leg motility before the embryos were sacrificed. It had been reported by us that the motility of normal chick embryos is periodic, activity phases alternating with inactivity phases. Both the overall activity, i.e., percent of activity during a standard 15-minute observation period, and the durations of activity and inactivity phases were found to be the same in experimental embryos and in control embryos with thoracic gaps, a t least up to and including 15-day embryos. Histological checks showed the complete absence of lumbar spinal ganglia i n the majority of embryos and, the presence of a few small thoracic ganglia in some cases. All embryos with lumbar ganglia were discarded. The motor roots formed a normal plexus, and the pure motor nerves emerging from it showed a normal peripheral distribution and muscle innervation. It is concluded that the leg motility results from autonomous discharges of the lateral motor or internuncial neurons, and that sensory input is not necessary for the triggering, the maintenance or the periodicity of the leg motility. A sharp decline of motility was observed i n 17-day embryos. A study of the histological condition of the residual spinal cord showed a numerical depletion and partial degeneration of the lateral motor column. This deterioration is considered to be responsible for the functional impairments.The implication of these results for the widespread notion that "self-stimulation" and similar "experiences" during embryonic development play a n important role in the molding of behavior is discussed. Dedicuted t o Dr. J . Holtfreter, o n the occasion o f his 65th birthdayIn previous publications (Hamburger, '63; Hamburger and Balaban, '63; Hamburger, '64; Hamburger, Balaban, Oppenheim and Wenger, '65) we have characterized the motility of the chick embryo as follows : ( 1 ) It begins at three and one-half days with a slight turning of the head at long intervals of approximately one minute and builds up to a peak of activity that is reached at 13 days, when the embryo is in motion for 80% of the time. ( 2 ) Motility is periodic; activity phases alternating with inactivity phases. ( 3 ) The movements are random movements of different parts of the body, with no obvious coordination of the parts. It was found furthermore that no triggers from higher centers are required for body movements. Following early embryonic isolation of the spinal cord from the brain, periodic body and li...

Spontaneous facial motility in infancy: A 3D kinematic analysis

“…Prenatal and early postnatal development is marked by spontaneous movement (Bekoff, 2001;Birnholz, Stephens, & Faria, 1978;de Vries, Visser, & Prechtl, 1982;Geerdink, Hopkins, Beek, & Heriza, 1996;Hall & Oppenheim, 1987;Hamburger, Wenger, & Oppenheim, 1966;Thelen, 1979). Most of the early investigations of spontaneous motility concluded that these movements serve an adaptive function in early development (Coghill, 1929;Hooker, 1944;Hamburger et al, 1966).…”

“…This view of early motor development is consistent with a conceptual shift within the developmental literature from descriptions that focus on ''forward reference'' systems (e.g., genetic determination) to those that emphasize the importance of sensorimotor experience in both neuronal and behavioral development (Edelman, 1987;Gottlieb, 1992;Kuo, 1967;Thelen, 1995). The earliest spontaneous movements are thought to be generated by endogenous neural activity (i.e., autonomous discharge of motor neurons), rather than from activity related to myogenics, reflexogenics, or descending input (Hamburger et al, 1966;Roeder, 1963). During early prenatal development, primitive motor neuron rootlets exhibit phasic spontaneous discharge prior to connecting to their target muscle fibers (Gust, Wright, Pratt, & Bosma, 2003) and myotubes contract as soon as they are innervated by motoneurons (Landmesser & Morris, 1975).…”

“…During early prenatal development, primitive motor neuron rootlets exhibit phasic spontaneous discharge prior to connecting to their target muscle fibers (Gust, Wright, Pratt, & Bosma, 2003) and myotubes contract as soon as they are innervated by motoneurons (Landmesser & Morris, 1975). In animals, spontaneous activity in the spinal nervous system has been observed to evolve even in the absence of cortical, subcortical, and afferent systems (Hamburger et al, 1966;Roeder, 1963). For example, spontaneous movements develop normally even when the entire dorsal half of the chick lumbosacral spinal cord is removed at 2-2.5 days (Hamburger et al, 1966).…”

“…In animals, spontaneous activity in the spinal nervous system has been observed to evolve even in the absence of cortical, subcortical, and afferent systems (Hamburger et al, 1966;Roeder, 1963). For example, spontaneous movements develop normally even when the entire dorsal half of the chick lumbosacral spinal cord is removed at 2-2.5 days (Hamburger et al, 1966).…”

Electrical Activity in the Spinal Cord of the Chick Embryo, in situ

“…These embryos showed normal patterns of leg motility at least up to 15 to 17 days. 5 Although the brain influences normal embryonic behavior,6 and sensory input may influence it, these recent experiments imply that autonomous activity of interneurons or motor neurons in the ventral half of the cord is sufficient to sustain motility up to about 15 to 17 days. On the 17th day, the spontaneous, uncoordinated motility of early stages declines and is superseded by a series of coordinated movements which lead to hatching of the chick on day 21.7 Sensory and brain inputs may be necessary for the execution of these late appearing, well organized movements.…”