Paul S.G. Stein - US grants

A rhythmic motor program, termed the scratch reflex, can be elicited by gentle mechanical stimulation of the shell in an immobilized, spinal turtle. Microelectrodes will be inserted into the somata of limb motor neurons in order to record the synaptic potentials controlling the activities of these cells. These recordings will reveal the output characteristics of the spinal cord generator for the scratch program. Manipulations of membrane voltage and cellular ionic content will allow us to explore the ionic mechanisms underlying these synaptic potentials. The descending neuronal signal driven by cutaneous afferents from the shell will be recorded and its effect on the scratch generator explored. Our hypothesis is that this decending signal may exhibit characteristics of "command" neurons found in invertebrates and fishes. The objectives of this work are to characterize the basic properties of turtle spinal cord neurons involved in the generation of motor programs. Since many features of spinal cord are invariant throughout the vertebrates, it is our hope that our results on turtle will serve as useful working hypotheses for the exploration of the motor mechanisms in more complex vertebrates.

The project to be performed examines neural mechanisms responsible for processing information coming from the skin and transforming that cutaneous information into an adaptive motor response. Dr. Paul Stein studies the scratch reflex, a complex behavior produced by the spinal cord. He has developed a spinal cord preparation that, in the absence of movement-related sensory feedback, selects which of the three distinct motor output patterns is an appropriate response to a tactile stimulus and generates that motor output pattern. The process of selection implies that a decision is made. Therefore, neural mechanisms for making motor decisions are intrinsic to the spinal cord. The goal of this project is to reveal these mechanisms.

Neuronal networks in the spinal cord of limbed vertebrates generate motor rhythms that usually include alternation between activation of hip flexor and hip extensor motoneurons. We study these rhythms in a spinal turtle with complete spinal cord transection just posterior to the forelimb enlargement. We examine spinal cord circuitry responsible for the production of 3 motor strategies, "forms", of scratching (rostral, pocket, caudal) and 2 forms of swimming (forward swim, backpaddle). We test the "bilateral shred core" hypothesis: spinal cord circuitry involved in the production of a specific rhythmic behavior in a hindlimb is bilaterally distributed and is responsible for the production of more than one rhythmic behavior. We developed a spinal preparation with transverse hemisection anterior to the hindlimb enlargement that produces hip flexor rhythms in the absence of hip extensor activity in response to ipsilateral stimulation in the mid-body rostral scratch receptive field (J Neurosci 18:467-479, 1998). This establishes that hip flexor circuits can be rhythmogenic in the absence of hip extensor circuit activation. This preparation also generates "reconstructed" normal rostral scratching with hip flexor/extensor rhythmic alternation in response to 2-site stimulation with one site in the intact-side rostral scratch receptive field and the other site in another scratch receptive field. These experiments support the bilateral shared core hypothesis for the 3 forms of the scratch. We propose experiments that study scratch motor patterns in the spinal immobilized turtle with transverse hemisection. We analyze this motor patterns along with synaptic drive in motoneurons and activity patterns of descending propriospinal interneurons. We test specific predictions of the bilateral shared core hypothesis, e.g., we examine post-synaptic potentials in contralateral hip motoneurons during scratching motor rhythms in response to tactile stimulation in an ipsilateral scratch receptive field. We also propose experiments that study scratching and swimming in a spinal turtle with movement. We measure muscle activity patterns and hindlimb kinematics. We test a version of the bilateral shared core hypothesis stating that neural elements that produce scratch rhythms also produce swim rhythms. Turtle spinal cord is similar to that of other vertebrates, including humans. The spinal mechanisms that we reveal in turtle serve as working hypotheses for studies of motor rhythm generation in other vertebrates, including humans.