Coupling of Efferent Neuromodulatory Neurons to Rhythmical Leg Motor Activity in the Locust

Abstract

The spike activity of neuromodulatory dorsal unpaired median (DUM) neurons was analyzed during a pilocarpine-induced motor pattern in the locust. Paired intracellular recordings were made from these octopaminergic neurons during rhythmic activity in hindleg motor neurons evoked by applying pilocarpine to an isolated metathoracic ganglion. This motor pattern is characterized by two alternating phases: a levator phase, during which levator, flexor, and common inhibitor motor neurons spike, and a depressor phase, during which depressor and extensor motor neurons spike. Three different subpopulations of efferent DUM neurons could be distinguished during this rhythmical motor pattern according to their characteristic spike output. DUM 1 neurons, which in the intact animal do not innervate muscles involved in leg movements, showed no change apart from a general increase in spike frequency. DUM 3 and DUM 3,4 neurons produced the most variable activity but received frequent and sometimes pronounced hyperpolarizations that were often common to both recorded neurons. DUM 5 and DUM 3,4,5 neurons innervate muscles of the hindleg and showed rhythmical excitation leading to bursts of spikes during rhythmic activity of the motor neurons, which innervate these same muscles. Sometimes the motor output was coordinated across both sides of the ganglion so that there was alternating activity between levators of both sides. In these cases, the spikes of DUM 5 and DUM 3,4,5 neurons and the hyperpolarization of DUM 3 and DUM 3,4 neurons occurred at particular phases in the motor pattern. Our data demonstrate a central coupling of specific types of DUM neurons to a rhythmical motor pattern. Changes in the spike output of these particular efferent DUM neurons parallel changes in the motor output. The spike activity of DUM neurons thus may be controlled by the same circuits that determine the action of the motor neurons. Functional implications for real walking are discussed.

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

“…At present we cannot rule out the possibility that OA is absorbed more readily than other amines. This caveat aside, our data are consistent with the critical role for OA in regulating motor behaviors in many invertebrates, in part by initiating the central pattern generators (CPGs) for crawling, walking, and flying (Sombati and Hoyle 1984;Hashemzadeh-Gargari and Friesen 1989;Ramirez and Pearson 1991;Orchard et al 1993;Baudoux et al 1998;Roeder 1999). Once initiated by OA or other modulatory neurotransmitters, CPGs propagate a stereotypic behavior independent of sensory input (Marder and Bucher 2001;Grillner 2003).…”

Expanding the Neuron's Calcium Signaling Repertoire: Intracellular Calcium Release via Voltage-Induced PLC and IP3R Activation

“…To test whether spiking patterns of DUM neurons, as occurring during normal behavior [17,18], were sufficient to produce [Ca 2+ ] i elevations in the absence of calcium influx, a similar protocol as depicted in Figure 1 was repeated under current clamp conditions (Figure 2). First, in calcium-containing saline, bursts of action potentials were induced by current injection of 500-ms duration just above firing threshold.…”

Modulation of Low-Voltage-Activated Inward Current Permeable to Sodium and Calcium by DARPP-32 Drives Spontaneous Firing of Insect Octopaminergic Neurosecretory Cells

“…It is also well established that DUM neurons are an important component of different motor networks (Burrows and Pflüger, 1995; Baudoux et al, 1998; Mentel et al, 2008; Vierk et al, 2009). Although DUM neurons may be activated by sensory stimuli (e.g., Baudoux and Burrows, 1998; Field et al, 2008; Pflüger et al, 2011; Rand et al, 2012), they are defined by the absence of common somatic synaptic inputs from presynaptic neurons and by their uncommon intrinsic property allowing adequate beating pacemaker activity (Grolleau and Lapied, 2000; Wicher et al, 2001; Defaix and Lapied, 2005; Heidel and Pflüger, 2006; Lavialle-Defaix et al, 2006; Gautier et al, 2008).…”