Electric fish use electrocommunication signals to fine tune relative dominance and access to resources

Social animals establish dominance hierarchies to regulate access to resources. Although communication signals could reduce costs in negotiating dominance, their detailed role and emergence in non-mammalian vertebrates is not well researched. We tracked electrocommunication signals and agonistic behaviors of the gymnotiform fish Apteronotus leptorhynchus in staged competition experiments. Subordinates emitted the majority of so called “rises” in dependence on the competitor’s relative size and sex. Rises provoked ritualized biting or chasing behaviors by dominant fish. Already after 25 minutes losers were accurately predictable based on rise numbers, but they continued to emit rises. We suggest the interplay between communication and aggression to fine tune relative dominance without questioning dominance rank. This communication system regulates the skewness of access to resources within a dominance hierarchy and allows A. leptorhynchus to populate neotropical rivers with high abundances.

Glutamatergic Control Of A Pattern-Generating Central Nucleus In A Gymnotiform Fish

ABSTRACTThe activity of pattern-generating networks (CPG) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. Gymnotus omarorum, a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. G. omarorum emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication. The EOD is considered the behavioral output of an electromotor CPG which, modulated by descending influences, organizes adaptive electromotor behaviors in response to environmental and social challenges. The CPG is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. We used electrophysiological and pharmacological techniques in brainstem slices of G. omarorum to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptors subtypes. We also show, for the first time in gymnotiformes, that glutamatergic control of the CPG likely involves both AMPA-NMDA receptors transmitting and only-NMDA segregated synapses contacting pacemaker cells. Our data shed light on the fast neurotransmitter control of a vertebrate CPG that seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs.NEW & NOTEWORTHYUnderpinnings of neuromodulation of pattern-generating central networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involve the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.

Cellular and network mechanisms may generate sparse coding of sequential object encounters in hippocampal-like circuits

In mammals, the localization of distinct landmarks is performed by hippocampal neurons that sparsely encode an animal’s location relative to surrounding objects. Similarly, the dorsal lateral pallium (DL) is essential for spatial learning in teleost fish. The DL of weakly electric gymnotiform fish receives sensory inputs from the preglomerular nucleus (PG), which has been hypothesized to encode the temporal sequence of electrosensory or visual landmark/food encounters. Here, we show that DL neurons have a hyperpolarized resting membrane potential combined with a high and dynamic spike threshold that increases following each spike. Current-evoked spikes in DL cells are followed by a strong small-conductance calcium-activated potassium channel (SK) mediated after-hyperpolarizing potential (AHP). Together, these properties prevent high frequency and continuous spiking. The resulting sparseness of discharge and dynamic threshold suggest that DL neurons meet theoretical requirements for generating spatial memory engrams by decoding the landmark/food encounter sequences encoded by PG neurons.

Dendritic SK channels convert NMDA-R-dependent LTD to burst timing-dependent plasticity

Feedback and descending projections from higher to lower brain centers play a prominent role in all vertebrate sensory systems. Feedback might be optimized for the specific sensory processing tasks in their target brain centers, but it has been difficult to connect the properties of feedback synapses to sensory tasks. Here, we use the electrosensory system of a gymnotiform fish ( Apteronotus leptorhynchus) to address this problem. Cerebellar feedback to pyramidal cells in the first central electrosensory processing region, the electrosensory lateral line lobe (ELL), is critical for canceling spatially and temporally redundant electrosensory input. The ELL contains four electrosensory maps, and we have previously analyzed the synaptic and network bases of the redundancy reduction mechanism in a map (centrolateral segment; CLS) believed to guide electrolocation behavior. In the CLS, only long-term depression was induced by pairing feedback presynaptic and pyramidal cell postsynaptic bursts. In this paper, we turn to an ELL map (lateral segment; LS) known to encode electrocommunication signals. We find remarkable differences in synaptic plasticity of the morphologically identical cerebellar feedback input to the LS. In the LS, pyramidal cell SK channels permit long-term potentiation (LTP) of feedback synapses when pre- and postsynaptic bursts occur at the same time. We hypothesize that LTP in this map is required for enhancing the encoding of weak electrocommunication signals. We conclude that feedback inputs that appear morphologically identical in sensory maps dedicated to different tasks, nevertheless display different synaptic plasticity rules contributing to differential sensory processing in these maps.