Periodic High-Conductance States in Spinal Neurons during Scratch-Like Network Activity in Adult Turtles

Abstract

Intense synaptic activity may alter the response properties of neurons in highly interconnected networks. Here we investigate whether the excitability and the intrinsic response properties of neurons in the spinal cord are affected by the increased synaptic conductance during functional network activity. Scratch episodes were induced by mechanical stimulation in the isolated carapace-spinal cord preparation from the adult turtle. Intracellular recordings revealed a dramatic increase in synaptic activity in interneurons and motoneurons during scratch activity. Superimposed slow depolarizing waves were phase-related to the rhythmic bouts of spike activity in the hip flexor nerve. The increase in synaptic conductance in interneurons and motoneurons varied with the scratch rhythm. During individual episodes, the conductance shifted smoothly with the scratch rhythm from near-resting levels to levels two to four times higher. In slice experiments, we found that even moderate increases in the conductance of motoneurons suppressed the slow afterhyperpolarization and the plateau potentials. We conclude that the excitability and the intrinsic response properties of spinal neurons are periodically quenched by high synaptic conductance during functional network activity.

Irregular Firing and High-Conductance States in Spinal Motoneurons during Scratching and Swimming

“…A similar increase in conductance was demonstrated in turtle motoneurons during scratch network activity (Robertson and Stein, 1988;Alaburda et al, 2005;Berg et al, 2008). To determine whether conductance increase in motoneurons extends to other spinal network activities, we compared conductance in the same motoneurons during scratch and swim network activity.…”

“…Red-eared turtles (Trachemys scripta elegans) were obtained from Nasco. Surgical procedures were described previously (Alaburda and Hounsgaard, 2003). Briefly, turtles (n ϭ 11, of either sex), 10 -15 cm carapace length, were placed on crushed ice 2 h before surgery to induce drowsiness and reduce stress and pain by hypothermia.…”

“…It was also thought that intrinsic properties of motoneurons would contribute to spike patterns in large-scale CPGs (Delgado-Lezama and Hounsgaard, 1999;Kiehn et al, 2000). This was challenged by the highconductance states observed in motoneurons during scratching in an ex vivo carapace-spinal cord preparation from adult turtles (Alaburda et al, 2005;Berg et al, 2007). Highconductance states were observed earlier in the cortex (BorgGraham et al, 1998;Paré et al, 1998;Destexhe et al, 2003) and are thought to mediate irregular firing (Softky and Koch, 1993;Holt et al, 1996).…”

“…Highconductance states were observed earlier in the cortex (BorgGraham et al, 1998;Paré et al, 1998;Destexhe et al, 2003) and are thought to mediate irregular firing (Softky and Koch, 1993;Holt et al, 1996). Furthermore, spinal motoneurons fire irregularly during scratching (Berg et al, 2007 due to increased synaptic fluctuations in membrane potential and shunting intrinsic properties (Alaburda et al, 2005;Berg et al, 2007). However, high-conductance states and irregular firing in motoneurons were observed during scratching, which is a highly specialized motor behavior.…”

Contribution of motoneuron intrinsic properties to fictive motor pattern generation

“…For example, in the absence of synaptic input, the motoneurons involved in fictive scratch in turtles exhibit largeamplitude voltage fluctuations in response to current injections, indicating that they possess complex intrinsic properties (Alaburda et al 2005). When the premotor network driving fictive scratch is activated, however, the voltage fluctuations observed are diminished because of the synaptic conductance impinging upon the motoneurons.…”