Wing mechanosensory modulation of optic flow-sensitive descending neurons in butterflies

Abstract

Visual motion processing in flying insects is strongly modulated by behavioural state, yet the mechanisms by which mechanosensory feedback contributes to this modulation remain poorly understood. Here we show that wing mechanosensation alone is sufficient to modulate a subset of optic-flow-sensitive descending neurons (WFDNs) in butterflies. Airflow stimulation of the wings, mimicking flight conditions, increased baseline firing rates and reduced response latencies in WFDNs, without altering response gain or temporal frequency tuning. These effects indicate that mechanosensory modulation acts through mechanisms distinct from those governing other state-dependent changes in visual processing. Consistent with this interpretation, previous work has shown that baseline firing and response latency can be rapidly modulated, whereas gain changes arise through slower neuromodulatory pathways. Mechanosensory modulation was cell-type specific: the horizontally tuned WFDNL neuron was consistently affected across individuals, whereas other WFDN types were largely insensitive, likely reflecting the unilateral airflow stimuli used here. Interestingly, WFDNL modulation arose exclusively from mechanosensory input from the proximal area of the wing, not from distal wing deformation. This suggests that descending visual pathways require only coarse gain or excitability modulation rather than detailed information about wing shape or strain, leaving fast reflexive control of distal wing deformation to local ganglionic circuits. Together, our results demonstrate that wing mechanosensation selectively modulates visual descending pathways by altering excitability and timing rather than visual feature encoding, supporting the existence of multiple, parallel mechanisms for state-dependent modulation of descending visual signals during flight.