Locomotor pattern generation requires the network coordination of spinal ventral horn neurons acting in concert with the oscillatory properties of individual neurons. In the spinal cord, N-methyl-D-aspartate (NMDA) activates neuronal oscillators that are believed to rely on Ca²⁺ entry to the cytosol through voltage operated Ca²⁺ channels and synaptically activated NMDA receptors. Ca²⁺ signaling in lamprey ventral horn neurons thus plays a determinant role in the regulation of the intrinsic membrane properties and network synaptic interaction generating spinal locomotor neural pattern activity. We have characterized aspects of this signaling quantitatively for the first time. Resting Ca²⁺ concentrations were between 87 and 120nM. Ca²⁺ concentration measured during fictive locomotion increased from soma to distal dendrites (from 208± 27nM in the soma to 335± 41nM in the proximal dendrites to 457 +/- 68nM in the distal dendrites). We sought to determine the temporal and spatial properties of Ca²⁺ oscillations, imaged with Ca²⁺-sensitive dyes and correlated with fluctuations in membrane potential, during lamprey fictive locomotion. The Ca²⁺ signals recorded in the dendrites showed a great deal of spatial heterogeneity. Rapid changes in Ca²⁺ induced fluorescence coincided with action potentials, which initiated significant Ca²⁺ transients distributed throughout the neurons. Ca²⁺ entry to the cytosol coincided with the depolarizing phase of the locomotor rhythm. During fictive locomotion larger Ca²⁺ oscillations were recorded in dendrites compared to somata in motoneurons and premotor interneurons. Ca²⁺ fluctuations were barely detected with dyes of lower affinity providing alternative empirical evidence that Ca²⁺ responses are limited to hundreds of nm during fictive locomotion.