Autoinhibition of serotonin cells: An intrinsic regulatory mechanism sensitive to the pattern of usage of the cells

Abstract

After periods of high-frequency firing, the normal rhythmically active serotonin (5HT)-containing neurosecretory neurons of the lobster ventral nerve cord display a period of suppressed spike generation and reduced synaptic input that we refer to as ''autoinhibition.'' The duration of this autoinhibition is directly related to the magnitude and duration of the current injection triggering the high-frequency firing. More interesting, however, is that the autoinhibition is inversely related to the initial firing frequency of these cells within their normal range of firing (0.5-3 Hz). This allows more active 5HT neurons to resume firing after shorter durations of inhibition than cells that initially fired at slower rates. Although superfused 5HT inhibits the spontaneous firing of these cells, the persistence of autoinhibition in saline with no added calcium, in cadmium-containing saline, and in lobsters depleted of serotonin suggests that intrinsic membrane properties account for the autoinhibition. A similar autoinhibition is seen in spontaneously active octopamine neurons but is absent from spontaneously active ␥-aminobutyric acid cells. Thus, this might be a characteristic feature of amine-containing neurosecretory neurons. The 5HT cells of vertebrate brain nuclei share similarities in firing frequencies, spike shapes, and inhibition by 5HT with the lobster cells that were the focus of this study. However, the mechanism suggested to underlie autoinhibition in vertebrate neurons is that 5HT released from activated or neighboring cells acts back on inhibitory autoreceptors that are found on the dendrites and cell bodies of these neurons.Biogenic amines appear to play key roles in the regulation of a wide array of physiological processes in both vertebrate and invertebrate nervous systems. They have been implicated in physiological processes and behaviors such as feeding (1), sleep (2, 3), repetitive motor acts such as locomotion (1), nociception (4), depression (5), and aggressive behavior, including the establishment of social hierarchies (6-9).In vertebrates, spontaneously active serotonergic neurons of the midline raphe nuclei are implicated in these behaviors, and these neurons have been the subject of many studies (for reviews, see refs. 10-12). These cells fire at slow rates between 0.5 and 3 Hz, depending on the state of wakefulness of the animal (1, 13-15). They generate large, approximately 60-mV, action potentials with prominent afterhyperpolarizations, which are likely to be mediated by calcium-activated potassium currents (10, 16). Both a high density of inhibitory somatodendritic type 1A 5-hydroxytryptamine (serotonin; 5HT 1A ) autoreceptors and the afterhyperpolarization are suggested to be important mechanisms for regulating the pacemaker activity of these cells (10, 17). Periods of high-frequency firing, experimentally evoked by electrical stimulation, are followed by a ''postactivation inhibition'' during which no action potentials are generated. The duration of the period of suppressed sp...

Ethological analyses of crayfish behavior: a new invertebrate system for measuring the rewarding properties of psychostimulants

“…[64]), but rather can be carried out on monoaminergic neurons that can be reliably identified between different subjects (e.g., ref. [24]). Recordings of DAcontaining neurons [57] in behaving crayfish may soon be possible [22].…”

“…[19,32]), making their use potentially ideal for studies of invertebrate drug reward. Due to their anatomical and physiological characteristics [8,24,37], as well as their accessibility to pharmaco-behavioral manipulations [28,47], monoamine neuromodulatory systems have received particular emphasis in previous research with decapod crustaceans. Furthermore, evidence for conserved, monoamine reuptake mechanisms in invertebrates [15,18,49] suggests the existence of the requisite sites of action (e.g., see ref.…”

Neural Circuit Reconfiguration by Social Status

“…The cells fire tonically at rates that differ between preparations from 0.5-3 Hz to 15 Hz (Heinrich et al, 1999). In semi-intact preparations from socially isolated and dominant animals (see Materials and Methods, above; Fig.…”

“…A bilaterally symmetric pair of anteriorly projecting, serotonin-containing neurons in the first abdominal ganglion, the A1 5-HT cells (Beltz and Kravitz, 1983;Real and Czternasty, 1990;Rossi-Durand, 1993;Heinrich et al, 1999), participates in the touch response. The A1 5-HT were identified from their shapes, discharge patterns, and immunoreactivity to serotonin antibody (see Methods and Materials, above).…”

Synaptic Connectivity of Amine-Containing Neurosecretory Cells of Lobsters: Inputs to 5HT- and OCT- Containing Neurons

“…The A1-5HT cells are reliably identified by their spontaneous spiking activity and the amplitude and shape of the action potential, which shows a pronounced hyperpolarizing afterpotential (Beltz and Kravitz, 1987;Ma et al, 1992;Hörner et al, 1997;Heinrich et al, 1999). Their endogeneous firing level is regulated by tonic inhibitory input, mainly coming from the A3 ganglion and to a lesser extent by unidentified excitatory synaptic inputs Weiger and Ma, 1993).…”