Weakly electric mormyrid fish can tune out their own “electric voice” and properly shift this internal filter in time with testosterone-driven changes.
Unlike most other animals’ mode of auditory communication, mormyrid fish possess the ability to communicate using pulses of electricity. The pulse waveform of this “electric voice” varies between individuals and can include information regarding the hormonal state of senders – that is to say, whether a male fish is in the mood for a mate.
In order to accurately perceive signals from nearby fish, mormyrids need a way to ignore their own electric chatter. That’s where the corollary discharge comes into play – a predictive motor system that is time-locked to tell the brain to briefly ignore self-signals and perceive only what’s coming in from the surrounding environment. However, changes in the external environment, much like those observed during the rainy breeding season, can trigger internal hormonal changes that alter the production and perception of electric signals.
A recent study from postdoctoral fellow Matasaburo Fukutomi and Professor Bruce Carlson of Washington University in St. Louis demonstrates that testosterone, which naturally elongates the waveform of ready-to-mate males during breeding season, also affects the timing of corollary discharge. Such a finding might lead to understanding hormonal effects on the link between sensory and motor systems.
Being able to distinguish between self and other is a common feature across the animal kingdom. The mechanisms of corollary discharge and the effects of hormones on motor output are well understood in the weakly electric mormyrid fish. This notion, and also having a communication system that is sensitive to the steroid hormone testosterone, makes them an excellent model organism for understanding seasonal adaptation via mechanisms of hormonal plasticity.
To understand seasonal adaptive behavior induced by hormonal changes, previous studies have investigated the effects of testosterone on the electric organ of mormyrid fish. Testosterone acts directly on the electric organ in male fish to elongate the electric organ discharge (EOD), indicating a readiness to breed. This new research, published in Current Biology, sheds light on how the hormone concurrently shifts corollary discharge to maintain accurate signal perception.
The study included two subject groups: one received testosterone while the other received a vehicle. The researchers first obtained individual EOD recordings from freely swimming fish. As previously observed, the fish exhibited an increased EOD duration following testosterone treatment. The next step was to record responses obtained from electroreceptors (Knollenorgans or KOs) located on the skin to electrosensory stimulation that mimicked self-generated EOD. In treated fish, there was a shift in the electroreceptors’ activity that was coordinated with EOD elongation.
KOs respond to EODs generated by both the individual and nearby fish and send this information to the electrosensory lateral line lobe (nELL) in the brain. The nELL also receives inhibitory signals from the corollary discharge pathway telling it to ignore any self-generated information. This now-filtered sensory information is then sent to the exterolateral nucleus (ELa), where the only signals perceived are the EODs from nearby fish. The timing of inhibition to nELL can be quantified from the timing of responses in ELa neurons (a lack of response indicates the inhibitory timeframe). The researchers found that this timeframe was delayed and elongated in testosterone treated fish, indicating a delay in the timing of corollary discharge.
Finally, the researchers needed a way to understand how time shifts in corollary discharge are matched with EOD elongation. Through a spinal cord transection, it is possible to electrically silence these fish. By doing so, sensory feedback from self-generated signals is eliminated. It was thought that this sensory feedback altered by a longer EOD might encourage the fish to learn the new signal duration and, therefore, shift its corollary discharge to match. However, there was no significant evidence to suggest that this was the case. Without feedback, the inhibition window from the corollary discharge pathway was delayed, with timing differences between silenced vehicle and testosterone groups similar to timing differences of intact fish. The lack of need for sensory feedback in the adjustment of timing suggests to the researchers that testosterone independently and synchronously affects the behavioral output of the electric organ and the timing of the internal corollary discharge pathway. The cellular mechanisms underlying hormonal effects on the timing of corollary discharge have yet to be determined, leaving future directions for this study wide open.
Maggie Stanford is a Neuroprep Postbacc Scholar in the lab of Bruce Carlson, PhD.