Rhythmicity of spinal neurons activated during each form of fictive scratching in spinal turtles

Abstract

Are behaviors that rely on common muscles and motoneurons generated by separate or overlapping groups of pattern-generating neurons? This question was investigated for the three forms of scratching in immobilized, spinal turtles. Individual neurons were recorded extracellularly from the gray matter through most of the spinal cord hindlimb enlargement gray matter, but were avoided in the region of motoneuron cell bodies. Each form of fictive scratching was elicited by mechanical stimulation of the body surface. The rhythmic modulation of spinal neurons was assessed using phase histograms and circular statistics. The degree of rhythmic modulation and the phase preference of each rhythmically active neuron were measured with respect to the activity cycle of the ipsilateral hip flexor nerve. The action potentials of rhythmic neurons tended to be concentrated in a particular phase of the ipsilateral hip flexor activity cycle no matter which form of fictive scratching was elicited. This consistent phase preference suggests that some of these neurons may contribute to generation of the hip rhythm for all three forms of scratching, strengthening the case that vertebrate pattern-generating circuitry for distinct behaviors can be overlapping. The degree of rhythmic modulation of each unit during fictive scratching was consistently correlated with the dorsoventral location of the recording, but not with the mediolateral or rostrocaudal location; neurons located more ventrally tended to be more rhythmic. The phase preferences of units were related to the region of the body surface to which each neuron responded maximally (i.e., the region to which each unit was broadly tuned). Units tuned to the rostral scratch or pocket scratch region tended to have a phase preference during ipsilateral hip flexor activity, whereas units tuned to the caudal scratch region did not. This suggests the hypothesis that the hip flexes further during rostral and pocket scratching, and extends further during caudal scratching, due to the net effects of a population of spinal interneurons that are both broadly tuned and rhythmically active.