1. Physics Department, University of Ottawa, Ottawa, Ontario K1N 6N5, Canada
2. Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada
3. Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019, USA

Correspondence to: Brent Doiron^1,2 Correspondence and requests for materials should be addressed to B.D.(e-mail: Email: bdoiron@science.uottawa.ca).

Abstract

Stimulus-induced oscillations occur in visual^{1, 2}, olfactory^{3, 4, 5, 6} and somatosensory⁷ systems. Several experimental^{2, 3, 5} and theoretical^{8, 9, 10, 11, 12, 13} studies have shown how such oscillations can be generated by inhibitory connections between neurons. But the effects of realistic spatiotemporal sensory input on oscillatory network dynamics and the overall functional roles of such oscillations in sensory processing are poorly understood. Weakly electric fish must detect electric field modulations produced by both prey (spatially localized)¹⁴ and communication (spatially diffuse)¹⁵ signals. Here we show, through in vivo recordings, that sensory pyramidal neurons in these animals produce an oscillatory response to communication-like stimuli, but not to prey-like stimuli. On the basis of well-characterized circuitry¹⁶, we construct a network model of pyramidal neurons that predicts that diffuse delayed inhibitory feedback is required to achieve oscillatory behaviour only in response to communication-like stimuli. This prediction is experimentally verified by reversible blockade of feedback inhibition that removes oscillatory behaviour in the presence of communication-like stimuli. Our results show that a sensory system can use inhibitory feedback as a mechanism to 'toggle' between oscillatory and non-oscillatory firing states, each associated with a naturalistic stimulus.