Population behavior and self-organization in the genesis of spontaneous rhythmic activity by developing spinal networks Michael J. O’Donovan and Nikolai Chub During development spinal networks generate recurring episodes of rhythmic bursting that can be recorded from motoneurons and interneurons. Optical imaging has identified a set of propriospinal interneurons that may be important in the production of this activity. These neurons are rhythmically active, are recurrently interconnected and have powerful projections to motoneurons. The excitability of this propriospinal network is depressed by activity and recovers in the interval between episodes. These and other observations have been formulated into a qualitative model in which population behavior and self-organization are responsible for the spontaneous activity generated by developing spinal networks. Key words: development / rhythm generation / self-organization / spinal cord ©1997 Academic Press Ltd IN RECENT YEARS it has become apparent that networks in many parts of the developing nervous system are spontaneously active. This activity appears to regulate several developmental processes but very little is known about its genesis. In this review we discuss the results of work in our laboratory on the production of spontaneous rhythmic activity by spinal networks of the developing chick embryo. This work has produced some unexpected results that are not consistent with models for rhythmogenesis based solely on cellular or fixed-network oscillators. Our findings have raised the possibility that the production of spontaneous activity is best understood as a population behavior of developing spinal networks rather than the product of a specialized rhythm generating circuitry. The nature of spontaneous activity in the developing spinal cord Motor activity in the chick embryo is a particularly attractive system for study because the development of movement in ovo has been studied comprehensively by observation 1 and by quantitative electromyog- raphy. 2 An important advantage of investigating embryonic motility is the ability to relate the develop- ing activity to the emergence of locomotor behavior in the hatched animal. Such studies provide a unique insight into the nature of the circuitry activated in the embryo and its relation to the networks underlying mature behavior. In ovo electromyography has shown that the basic patterns of muscle activation that characterize adult locomotion appear early in devel- opment. This observation has led to the idea that the spinal networks active in the embryo are the pre- cursors of adult locomotor circuits. 2,3 For technical reasons it has not been possible to study the cellular and synaptic mechanisms responsi- ble for the production of embryonic movements in ovo . However, progress towards this goal has been accomplished using an isolated preparation of the chick embryo spinal cord. 4 This preparation gen- erates spontaneous activity which is similar, although not identical, to that produced in ovo but which is more amenable to experimental investigation than the intact embryo. Definition of terms The activity we will discuss in this review can be recorded from the ventral roots, muscle nerves or from individual neurons of the isolated spinal cord. 5 It comprises spontaneously recurring episodes or bouts of activity whose character and frequency vary with age. An ‘ episode ’ is a periodically recurring event that comprises a variable number of ‘ cycles’ of activity (see Figure 1A). When recorded intracellularly from motoneurons, From the Section on Developmental Neurobiology, Laboratory of Neural Control, NINDS, NIH, Building 49, Room 3A50, Bethesda, MD20892, USA seminars in CELL &DEVELOPMENTAL BIOLOGY, Vol 8, 1997: pp 21–28 ©1997 Academic Press Ltd 1084-9521/97/010021 + 08 $25.00/0/sr960117 21