Central pattern generators in the turtle spinal cord: selection among the forms of motor behaviors.

Neuronal networks in the turtle spinal cord have considerable computational complexity even in the absence of connections with supraspinal structures. These networks contain central pattern generators (CPGs) for each of several behaviors, including three forms of scratch, two forms of swim, and one form of flexion reflex. Each behavior is activated by a specific set of cutaneous or electrical stimuli. The process of selection among behaviors within the spinal cord has multisecond memories of specific motor patterns. Some spinal cord interneurons are partially shared among several CPGs, whereas other interneurons are active during only one type of behavior. Partial sharing is a proposed mechanism that contributes to the ability of the spinal cord to generate motor pattern blends with characteristics of multiple behaviors. Variations of motor patterns, termed deletions, assist in characterization of the organization of the pattern-generating components of CPGs. Single-neuron recordings during both normal and deletion motor patterns provide support for a CPG organizational structure with unit burst generators (UBGs) whose members serve a direction of a specific degree of freedom of the hindlimb, e.g., the hip-flexor UBG, the hip-extensor UBG, the knee-flexor UBG, the knee-extensor UBG, etc. The classic half-center hypothesis that includes all the hindlimb flexors in a single flexor half-center and all the hindlimb extensors in a single extensor half-center lacks the organizational complexity to account for the motor patterns produced by turtle spinal CPGs. Thus the turtle spinal cord is a valuable model system for studies of mechanisms responsible for selection and generation of motor behaviors. NEW & NOTEWORTHY The concept of the central pattern generator (CPG) is a major tenet in motor neuroethology that has influenced the design and interpretations of experiments for over a half century. This review concentrates on the turtle spinal cord and describes studies from the 1970s to the present responsible for key developments in understanding the CPG mechanisms responsible for the selection and production of coordinated motor patterns during turtle hindlimb motor behaviors.

Modular organization of the multipartite central pattern generator for turtle rostral scratch: knee-related interneurons during deletions.

Central pattern generators (CPGs) are neuronal networks in the spinal cord that generate rhythmic patterns of motor activity in the absence of movement-related sensory feedback. For many vertebrate rhythmic behaviors, CPGs generate normal patterns of motor neuron activities as well as variations of the normal patterns, termed deletions, in which bursts in one or more motor nerves are absent from one or more cycles of the rhythm. Prior work with hip-extensor deletions during turtle rostral scratch supports hypotheses of hip-extensor interneurons in a hip-extensor module and of hip-flexor interneurons in a hip-flexor module. We present here single-unit interneuronal recording data that support hypotheses of knee-extensor interneurons in a knee-extensor module and of knee-flexor interneurons in a knee-flexor module. Members of knee-related modules are not members of hip-related modules and vice versa. These results in turtle provide experimental support at the single-unit interneuronal level for the organizational concept that the rostral-scratch CPG for the turtle hindlimb is multipartite, that is, composed of more than two modules. This work, when combined with experimental and computational work in other vertebrates, does not support the classical view that the vertebrate limb CPG is bipartite with only two modules, one controlling all the flexors of the limb and the other controlling all the extensors of the limb. Instead, these results support the general principle that spinal CPGs are multipartite.

Molecular, genetic, cellular, and network functions in the spinal cord and brainstem.

Studies of the model systems of spinal cord and brainstem reveal molecular, genetic, and cellular mechanisms that are critical for network and behavioral functions in the nervous system. Recent experiments establish the importance of neurogenetics in revealing cellular and network properties. Breakthroughs that utilize direct visualization of neuronal activity and network structure provide new insights. Major discoveries of plasticity in the spinal cord and brainstem contribute to basic neuroscience and, in addition, have promising therapeutic implications.

Alternation of agonists and antagonists during turtle hindlimb motor rhythms.

In a variety of vertebrates, including turtle, many classical and contemporary studies of spinal cord neuronal networks generating rhythmic motor behaviors emphasize a Reciprocal Model with alternation of agonists and antagonists, alternation of excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs), and reciprocal inhibition. Some studies of spinal cord neuronal networks, including some in turtle during scratch motor rhythms, describe a Balanced Model with concurrent EPSPs and IPSPs. The present report reviews turtle spinal cord studies and concludes that there is support for a Combined Model with both alternating and concurrent excitation and inhibition, that is, characteristics of both the Reciprocal and the Balanced Models, in the same spinal cord neuronal network for scratch reflex in turtle. Studies of spinal cord neuronal networks for locomotion in a variety of vertebrates also support a Combined Model.

Motor pattern deletions and modular organization of turtle spinal cord.

The turtle spinal cord contains a central pattern generator (CPG) that produces rhythmic hindlimb motor patterns during a rostral scratch. This review describes evidence in support of the hypothesis that the turtle rostral scratch CPG has a modular structure similar to that described in the Unit-Burst-Generator hypothesis for cat locomotion by Grillner. During normal rostral scratch in turtle, activity bursts rhythmically alternate with quiescence for each motor neuron pool; agonist activity rhythmically alternates with antagonist activity at each degree of freedom, e.g., hip, knee; and a transition from knee flexor to knee extensor motor neuron activity occurs midway during each hip flexor motor neuron burst. Hip extensor deletions, knee flexor deletions, and knee extensor deletions are motor pattern variations of rostral scratch. During each of these variations, agonist activity is rhythmic; antagonist activity and agonist quiescence are absent. Several classes of evidence during both normal and variation motor patterns support a modular organization of the turtle rostral scratch CPG: electroneurographic recordings from axons of motor neurons, intracellular recordings of synaptic potentials in motor neurons, and extracellular unit recordings from spinal interneurons. These data support the hypotheses that the knee extensor module is different from the hip extensor module and that the knee flexor module is different from the hip flexor module. Potential mechanisms for rhythmogenesis include reciprocal connections between agonist and antagonist modules at each degree of freedom, and agonist module rhythmogenesis. Additional tests of the modular hypothesis for turtle rostral scratch include unit recordings from knee-related interneurons during normal rostral scratch, as well as during knee-related deletions.

Variations in motor patterns during fictive rostral scratching in the turtle: knee-related deletions.

Agonist motor neurons usually alternate between activity and quiescence during normal rhythmic behavior; antagonist motor neurons are usually active during agonist motor neuron quiescence. During an antagonist deletion, a naturally occurring motor-pattern variation, there is no antagonist activity and no quiescence between successive bursts of agonist activity. Motor neuron recordings of normal fictive rostral scratching in the turtle displayed rhythmic alternation between activity and quiescence for hip flexors, knee flexors, and knee extensors. Knee-flexor activity occurred during knee-extensor quiescence. During a hip-extensor deletion, a variation of rostral scratching, rhythmic hip-flexor bursts occurred without intervening hip-flexor quiescence. There were 3 distinct patterns of knee motor activity during the cycle before or after a hip-extensor deletion. In most cycles, there was knee flexor-extensor rhythmic alternation. In some cycles, termed knee-flexor deletions, there was no knee-flexor activity and rhythmic knee-extensor bursts occurred without intervening knee-extensor quiescence. In other cycles, termed knee-extensor deletions, there was no knee-extensor activity and rhythmic knee-flexor bursts occurred without intervening knee-flexor quiescence. The concept of a module refers to a population of motor neurons and interneurons with similar activity patterns; interneurons in a module coordinate agonist and antagonist motor neuron activities, either with excitation of agonist motor neurons and interneurons, or with inhibition of antagonist motor neurons and interneurons. Previous studies of hip-extensor deletions support the concept of a rhythmogenic hip-flexor module. The knee-related deletions described here support the concept of rhythmogenic knee-flexor and knee-extensor modules linked by reciprocal inhibition.

Timing of knee-related spinal neurons during fictive rostral scratching in the turtle.

Knee-flexor motor activity rhythmically alternated with knee-extensor motor activity during fictive rostral scratching in the spinal turtle. A critical transition from knee-flexor motor activity to knee-extensor motor activity occurred during hip-flexor motor activity. A key feature of this transition was that the end-phases of knee-flexor motor activity were positively correlated with the start-phases of knee-extensor motor activity. We studied spinal interneurons with activities related to this transition. We previously used single-unit recording techniques to characterize a data set of descending propriospinal interneurons during rostral scratching. We focused here on a group of interneurons from this data set with start-phases (on-units) or with end-phases (off-units) near the start of knee-extensor motor activity. We showed that, for a subset of these units, the start-phases of on-units and the end-phases of off-units were positively correlated with the start-phases of knee-extensor motor activity. We present the hypothesis that some of these knee-related on- and off-units may play a role in timing knee motor activity during rostral scratching.

Modular organization of turtle spinal interneurons during normal and deletion fictive rostral scratching.

During normal rostral scratching in the spinal turtle, there is rhythmic alternation between hip-flexor and hip-extensor motor activity. During rostral scratching with hip-extensor deletions, there are successive bursts of hip-flexor motor activity and no activity in hip-extensor motor neurons. We characterized the ON- and OFF-phases of 72 descending propriospinal interneurons with distinct activity bursts during normal rostral scratching. We also studied the activity of these interneurons during deletion scratching. Hip-extensor interneurons were active when hip-flexor motor neurons were quiet in normal scratching and had zero overlap with hip-flexor motor activity. This population of hip-extensor interneurons, termed the hip-extensor module or hip-extensor unit-burst generator, was mainly quiet during deletion scratching. Our observation supports the concept that a module is a neuronal population that may be active or quiet in a coordinated manner during a spinal motor rhythm. During normal scratching, hip-flexor interneurons were active during hip-flexor motor activity, and spanning interneurons were active during both hip-flexor motor activity and quiescence. Hip-flexor and spanning interneurons with intermediate overlap with hip-flexor motor activity fired in bursts during deletion scratching. Hip-flexor and spanning interneurons with large overlap with hip-flexor motor activity fired continuously during deletion scratching. Key features of hip-flexor and spanning interneuron firing during normal scratching were preserved during deletion scratching. Thus these features do not require activity in the hip-extensor module in every cycle of a motor rhythm.