Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

Abstract

. Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator-and activity-deprived adult neural network. J Neurophysiol 90: 2720 -2730, 2003. First published July 2, 2003 10.1152/jn.00370.2003. The pyloric rhythm of the stomatogastric ganglion of the crab, Cancer borealis, slows or stops when descending modulatory inputs are acutely removed. However, the rhythm spontaneously resumes after one or more days in the absence of neuromodulatory input. We recorded continuously for days to characterize quantitatively this recovery process. Activity bouts lasting 40 -900 s began several hours after removal of neuromodulatory input and were followed by stable rhythm recovery after 1-4 days. Bout duration was not related to the intervals (0.3-800 min) between bouts. During an individual bout, the frequency rapidly increased and then decreased more slowly. Photoablation of back-filled neuromodulatory terminals in the stomatogastric ganglion (STG) neuropil had no effect on activity bouts or recovery, suggesting that these processes are intrinsic to the STG neuronal network. After removal of neuromodulatory input, the phase relationships of the components of the triphasic pyloric rhythm were altered, and then over time the phase relationships moved toward their control values. Although at low pyloric rhythm frequency the phase relationships among pyloric network neurons depended on frequency, the changes in frequency during recovery did not completely account for the change in phase seen after rhythm recovery. We suggest that activity bouts represent underlying mechanisms controlling the restructuring of the pyloric network to allow resumption of an appropriate output after removal of neuromodulatory input.

Neuromodulators, Not Activity, Control Coordinated Expression of Ionic Currents

“…After ϳ24 h, current densities were measured. At this point, the decentralized preparations have entered the so-called bouting stage of irregular pyloric activity, described by Luther et al (2003) or, in some cases, fully recovered their pyloric rhythmic activity (Fig. 1, decentralized day 1 and 4).…”

“…To remove the neuromodulatory inputs to the STG (decentralization), either the stn was transected or action potential transmission along the nerve was blocked by adding isotonic (750 mM) sucrose plus 0.1 M TTX to a Vaseline well built around the stn (Luther et al, 2003). The method of decentralization did not affect the results.…”

“…These inputs can be experimentally interrupted in vitro by blocking action potential transmission along the single neuromodulatory input nerve (stn) to the STG (henceforth referred to as decentralization) (Luther et al, 2003). Pyloric activity is temporarily interrupted immediately after decentralization but can recover to near control levels hours to days later (Thoby-Brisson and Simmers, 1998;Golowasch et al, 1999b;Luther et al, 2003).…”

“…Despite this variability, neurons and neural networks can maintain remarkable functional stability under variable conditions (Davis, 2006), can restore their functional levels of activity after perturbations and injury (Thoby-Brisson and Simmers, 1998;Luther et al, 2003;Saghatelyan et al, 2005), and sometimes show great similarity of activity patterns across individuals (Bucher et al, 2005). It is therefore important to understand how this conductance variability can result in stable activity.…”

Animal-to-Animal Variability in Motor Pattern Production in Adults and during Growth

“…However, the different correlations of phase values and cycle period may indicate that different animals have found different combinations of membrane and synaptic currents that give rise to very similar motor patterns. There is experimental evidence that stability of pyloric neuron activity results from activity-dependent homeostatic regulation, both at the level of single neurons (Turrigiano et al, 1994), and on the network level Simmers, 1998, 2000;Golowasch et al, 1999b;Luther et al, 2003). Previous theoretical work has shown that simple homeostatic rules in which Ca 2ϩ concentrations are used to track activity patterns can regulate both intrinsic properties and synaptic strengths (LeMasson et al, 1993;Liu et al, 1998;Golowasch et al, 1999b;Soto-Trevino et al, 2001).…”