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Neuropeptide-mediated temporal sensory filtering in a primordial nervous system

Wyss, L. S.; Bray, S. R.; Wang, B.

2024-12-19 animal behavior and cognition
10.1101/2024.12.17.628859 bioRxiv
Show abstract

Sensory filtering - prioritizing relevant stimuli while ignoring irrelevant ones - is crucial for animals to adapt and survive in complex environments. While this phenomenon has been primarily studied in organisms with complex nervous systems, it remains unclear whether simpler organisms also possess such capabilities. Here, we studied temporal information processing in Schmidtea mediterranea, a freshwater planarian flatworm with a primitive nervous system. Using long-term behavioral imaging and oscillatory ultraviolet (UV) light stimulations with rhythms matching the timescale of the animals short-term memory ([~]minutes), we observed that planarians initially ignored rhythmic oscillations in UV intensity but eventually began tracking them after several cycles, demonstrating sensory filtering. We identified two neuropeptides, knockdown of which eliminated the initial ignoring phase and led to immediate stimulus-tracking, suggesting that these neuropeptides mediate an active sensory gating mechanism preventing response to transient fluctuations in stimuli. Notably, when UV stimulation was coupled with synchronous visible light oscillations, the planarians tracked the combined signals immediately, indicating that coherence across sensory modalities can override the initial gating. Our findings demonstrate that even simple nervous systems can filter temporal information and that this mechanism is mediated by neuropeptides. Unlike classical fast-acting small-molecule neurotransmitters, neuropeptides provide a slower, sustained, and global form of modulation that allows for more sophisticated control of sensory processing. Significance statementWe show that simple nervous systems can use specific neuropeptides to achieve sensory filtering, a behavior previously thought to require complex brain architecture. This neuropeptide-mediated sensory gating mechanism reveals a fundamental role for neuropeptides in temporal information processing, offering insights into the mechanistic and evolutionary origins of attention-like behaviors.

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