Global Electrosensory Oscillations Enhance Directional Responses of Midbrain Neurons inEigenmannia

Abstract

. Eigenmannia, a genus of weakly electric fish, exhibits a specialized behavior known as the jamming avoidance response (JAR). The JAR results in a categorical difference between Eigenmannia that are in groups of conspecifics and those that are alone. Fish in groups exhibit the JAR behavior and thereby experience ongoing, global synchronous 20-to 50-Hz electrosensory oscillations, whereas solitary fish do not. Although previous work has shown that these ongoing signals do not significantly degrade electrosensory behavior, these oscillations nevertheless elicit short-term synaptic depression in midbrain circuits. Because short-term synaptic depression can have profound effects on the transmission of information through synapses, we examined the differences in intracellularly recorded responses of midbrain neurons in awake, behaving fish to moving electrosensory images under electrosensory conditions that mimic solitary fish and fish in groups. In solitary conditions, moving objects elicited Gaussian or sinusoidal postsynaptic potentials (PSPs) that commonly exhibited preferential responses to a direction of motion. Surprisingly, when the same stimulus was presented in the presence of the global oscillations, directional selectivity was increased in all neurons tested. The magnitudes of the differences in PSP amplitude for preferred and nonpreferred directions were correlated with a measure of short-term synaptic depression in both conditions. The electrosensory consequences of the JAR appear to result in an enhancement of the representation of direction of motion in midbrain neurons. The data also support a role for short-term synaptic depression in the generation and modulation of directional responses.

Routing the Flow of Sensory Signals Using Plastic Responses to Bursts and Isolated Spikes: Experiment and Theory

“…An electrode pair placed further away on both sides of the fish's body was used to deliver global stimulus. This stimulus consisted of highfrequency amplitude modulations (40 -60 Hz), consistent with the spatiotemporal content of electrosensory signals from nearby conspecifics (Tan et al, 2005;Ramcharitar et al, 2006;Stamper et al, 2010). ELL pyramidal cells consist of two major categories: E-and I-cells (Bell and Maler, 2005).…”

“…The spatiotemporal content of electrosensory modulations depends on the source of these signals. Electric fish aggregate in small groups under a wide range of behavioral and environmental contexts, including prey capture behavior, resulting in ongoing high-frequency RAMs that are global in nature (Ramcharitar et al, 2006;Stamper et al, 2010). In such complex sensory environments, the electrosensory receptor array is likely activated by simultaneous local and global stimuli.…”

Differences in the Time Course of Short-Term Depression Across Receptive Fields Are Correlated With Directional Selectivity in Electrosensory Neurons

“…The surgical and experimental procedures have been described in detail elsewhere (Bastian et al 2002;Chacron 2006;Chacron and Bastian 2008;Ramcharitar et al 2006;Rose and Fortune 1996;Toporikova and Chacron 2009) and were approved by the respective institutional animal care and use committees of the Marine Biological Laboratory, McGill University, and Johns Hopkins University. Animal husbandry and all experimental procedures followed guidelines established by the Society for Neuroscience and the National Research Council.…”

“…Stimuli included moving objects (Ramcharitar et al 2005(Ramcharitar et al , 2006) and electrical signals from both moving and stationary dipoles (Bastian et al 2002;Chacron 2006;Chacron et al 2003). The moving object consisted either of a 1.8-cm-wide metal plate with a plastic coating on the side opposite to the animal or of a dipole emitting a constant stimulus (see following text) that was actuated with a pen plotter (HP 7010B) and moved sinusoidally along the fish's rostrocaudal axis over a distance of 20 cm.…”

Perception and coding of envelopes in weakly electric fishes

“…In this regard, small prey items typically lead to low frequency (<10Hz) AMs (Nelson and MacIver, 1999;MacIver et al, 2001), whereas those caused by interaction with conspecifics lead to AMs with a wide frequency range (near 0Hz to 400Hz) (Heiligenberg, 1991;Zupanc and Maler, 1993;Ramcharitar et al, 2005;Tan et al, 2005;Ramcharitar et al, 2006).…”