Xenopus embryonic spinal neurons recorded in situ with patch‐clamp electrodes – conditional oscillators after all?

Abstract

The central pattern generator for swimming Xenopus embryo is organized as two half-centres linked by reciprocal inhibition. Microelectrode recordings suggest that Xenopus neurons are poorly excitable, necessitating a key role for postinhibitory rebound in the operation of the central pattern generator. However the Xenopus central pattern generator seems unusual in that the component neurons apparently have no intrinsic or conditional rhythmogenic properties. We have re-examined the firing properties of Xenopus embryo spinal neurons by making patch-clamp recordings in situ from intact spinal cord. Recordings made from 99 neurons were divided into three groups. Central pattern generator neurons overwhelmingly (44/51) fired trains of action potentials in response to current injection. Just over half of the sensory interneurons (13/22) also fired trains of action potentials. Neurons that received no synaptic inputs during swimming mostly fired just one or two action potentials (22/26). Thirty-four neurons were identified morphologically. Commissural (8/12) and descending (6/6) interneurons, key components of the spinal central pattern generator, fired repetitive trains of action potentials during current injection. Neurons that were not part of the central pattern generator did not demonstrate this preponderance for repetitive firing. Analysis of the interspike intervals during current injection revealed that the majority of central pattern generators, descending and commissural interneurons, could readily fire at frequencies up to twice that of swimming. We suggest that Xenopus neurons can be considered as conditional oscillators: in the presence of unpatterned excitation they exhibit an ability to fire rhythmically. This property makes the Xenopus embryonic central pattern generator more similar to other model central pattern generators than has hitherto been appreciated.

Role of type-specific neuron properties in a spinal cord motor network

“…More recent, in situ whole-cell recordings show that different spinal neuron types have type-specific properties that include different spike firing properties (Aiken et al, 2003;Li et al, 2002Li et al, , 2003Li et al, , 2004b. There is broad agreement about the spike firing characteristics of RB sensory neurons, Fig.…”

“…As a result, their firing is suppressed, sensory transmission is gated out and network behaviour is unaffected sensory pathway interneurons and reciprocal inhibitory cIN interneurons. However, Aiken et al (2003) suggest that excitatory CPG dINs fire repetitively on the basis of recordings from 5 neurons identified by activity during swimming and possession of a descending axon. In contrast, our evidence shows that dINs fire a single characteristically long-duration spike to current (Li et al, 2006).…”

“…Neurons of one type (cINs) exhibit a delayed burst in response to constant input current (Aiken et al, 2003); see Fig. 4(B) in Li et al (2004c).…”

Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord

“…Recently, the whole-cell patch technique has opened up the prospect of detailed understanding in the zebrafish and frog (Saint-Amant and Drapeau, 2001;Li et al, 2002;Aiken et al, 2003). At last, spinal interneuron functions can be related to their anatomy.…”

Persistent Responses to Brief Stimuli: Feedback Excitation among Brainstem Neurons

“…When depolarizing current was injected, while recording in 1 mM Mg 2ϩ saline, individual hdINs generally fired a single action potential, even at currents well above threshold (Fig. 4 A), like some other Xenopus spinal neurons (Aiken et al, 2003) and some mammal dorsal horn neurons (Prescott and De Koninck, 2002). At the end of current pulses, the membrane potential returned quickly to near rest with no evidence of any depolarizing plateau potential that outlasted the injected current (Kiehn, 1991).…”