Hormonal coordination of peripheral motor output and corollary discharge in a communication system

Abstract

Steroid hormones remodel neural networks to induce developmental or seasonal changes in animal behavior, but little is known about hormonal modulation of sensorimotor integration. Here, we investigate hormonal effects on a predictive motor signal, termed corollary discharge, that modulates sensory processing in weakly electric mormyrid fish. In the electrosensory pathway mediating communication behavior, inhibition activated by a corollary discharge precisely blocks sensory responses to self-generated electric pulses, allowing the downstream circuit to selectively analyze communication signals from nearby fish. These electric pulses are elongated by increasing testosterone levels in males during the breeding season. Using systematic testosterone treatment, we induced electric-pulse elongation in fish and found that the timing of electroreceptor spiking responses to self-generated pulses (reafference) was delayed as electric pulse duration increased. Recording evoked potentials from a midbrain electrosensory nucleus revealed that the timing of corollary discharge inhibition was delayed and elongated by testosterone. Further, this shift in corollary discharge timing was precisely matched to the shift in timing of the reafferent spikes. We then asked whether the shift in inhibition timing was caused by direct action of testosterone on the corollary discharge circuit or plasticity of the circuit through altered sensory feedback. We surgically silenced the electric organs of fish and found similar hormonal modulation of corollary discharge timing between intact and silent fish, suggesting that sensory feedback was not required for this shift. These results demonstrate that testosterone directly and independently modulates peripheral motor output and a predictive motor signal in a coordinated manner. SignificanceSelf-other discrimination is essential for animals. Internal predictive motor signals, or corollary discharge, provide motor information to sensory areas so that animals can perceive self- and other-generated stimuli differently. As behavior and associated sensory feedback change with development, corollary discharge must adjust accordingly. Using weakly electric mormyrid fish, we show that the steroid hormone testosterone alters electric signaling behavior and the resulting sensory feedback, as well as the timing of corollary discharge, to precisely match the altered sensory feedback. We also found that the altered sensory feedback itself is not necessary to drive this corollary discharge modulation. Our findings demonstrate that testosterone directly and independently regulates peripheral motor output and corollary discharge in a coordinated manner.