Effects induced by an actin-polymerizing peptide in goldfish mauthner neurons

Abstract

In goldfishes, we studied (i) manifestations of functional activity of Mauthner neurons (MNs) reflected in motor behavior and (ii) changes in 3-D morphometry (ratio of volumes) and ultrastructure of MNs after applications of an actin-polymerizing peptide obtained from scorpion venom and after vestibular rotational stimulations (trainings) inducing natural modification of functions of the MNs (adaptation). In MNs subjected to application of the peptide, the increase in the functional resistance and morphological stability caused by long-lasting stimulation directly depended on the dose of the applied peptide or on the effectiveness of trainings, whereas in intact and control MNs such stimulation resulted in significant decreases in the activity and volumes of these cells. At the ultrastructure level, both applications of the peptide and trainings caused the formation of extensive bundles of actin filaments ("stress-fibers") in the cytoplasm of MNs and led to an increase in the dimension of desmosome-like contacts (DLCs) in afferent synapses. At chemical synapses, the effect looked like a reciprocal decrease in the length of the active zones (a structural sign of long-term depression, LTD), while at mixed synapses this was manifested in an increase in the number of fibrillar bridges in the gaps of DLCs (a structural sign of long-term potentiation, LTP). The data obtained allow us to hypothesize that LTD of the efficacy of transmission through chemical synapses is involved in the formation of the adaptation state of the MNs and that polymerization of actin in the cytoplasm and DLCs underlies the mechanism of LTD and adaptation. The development of ultrastructural manifestations of LTP at mixed synapses after polymerization of actin by the peptide, which is related to a reciprocal increase in the efficacy of "mixed" afferent inputs, explains the maintenance of a high integral level of activity of the MNs, despite a drop in the functional activity of "chemical" afferent inputs. Therefore, the actin cytoskeleton plays a clearly significant role in the maintenance of the balance of excitation at the neuronal level.

Stabilization of motor asymmetry in the goldfish under the influence of optokinetic stimulation

“…In this case, the numbers of turnings of the fish per minute (an index indirectly characterizing the functional activity of MNs) were 6.27 ± 2.60 and 6.10 ± 2.09, respectively (B). In other words, the activity of MNs after vestibular stimulation of the individuals adapted due to training visual stimulation did not drop in a way usually observed in fishes adapted with respect to long-lasting vestibular stimulation [10]. In intact fishes, such vestibular stimulation led to more significant modifications of the motor asymmetry (their MAC changed from 0.58 ± 0.06 to 0.20 ± 0.20; n = 3).…”

“…were shown to correlate with its external morphology [24,25]. Experimental "strengthening" of the neuronal actin cytoskeleton results in an increase in the morphofunctional stability of the neuron [10].…”

“…There are indications that the actin cytoskeleton of MNs integrates the influences of synapses different in nature, provides the formation of adequate integral responses, and maintains the balance of the activity at different modes of functioning [29]. Due to "strengthening" of actin because of its polymerization, an increase in the resistivity of MNs is provided upon induction of adaptation to vestibular stimulation and after applications of dopamine or a peptide exerting a direct polymerizing effect on neuronal actin [10,11,30]. Therefore, it is logical to suppose that strengthening of the resistivity of motor asymmetry in the goldfish with respect to fatiguing COS using a series of training visual stimulation sessions is related to morphological "strengthening" of the ventral dendrite of the MN determined by the respective rearrangement of the state of dendroplasmic actin.…”

“…They are, to a considerable extent, determined, on the one hand, by the morphofunctional asymmetry of MNs that is manifested in behavior as the motor asymmetry of the fish [7,8] and, on the other hand, by variations of this asymmetry depending on the preceding loading on one afferent input or another. It was found that experimental adequate stimulation or unilateral elimination of one input selectively influences the structure and function of the individual MN; this leads to a change in the inborn motor asymmetry of the fish [9,10]. Regulation of all the above modifications at the level of the individual MN has not at present been studied.…”

Effects of optokinetic stimulation on motor asymmetry in the goldfish

“…Different techniques of natural stimulation (both selective and in combination with other influences) were for a long time extensively used in studies of the role of the MN lateral dendrite. Such experimental approaches allowed experimenters to obtain valuable findings [9,17,18]. At the same time, comparable approaches have not been developed with respect to the ventral dendrite of MNs.…”