Multisensory neural integration of chemical and mechanical signals

Abstract

Chemosensation and mechanosensation cover an enormous spectrum of processes by which animals use information from the environment to adapt their behavior. For pragmatic reasons, these sensory modalities are commonly investigated independently. Recent advances, however, have revealed numerous situations in which they function together to control animals' actions. Highlighting examples from diverse vertebrates and invertebrates, we first discuss sensory receptors and neurons that have dual roles in the detection of chemical and mechanical stimuli. Next we present cases where peripheral chemosensory and mechanosensory pathways are discrete but intimately packaged to permit coordinated reception of external cues. Finally, we consider how chemical and mechanical signals converge in central neural circuitry to enable multisensory integration. These insights demonstrate how investigation of the interplay between different sensory modalities is key to a more holistic and realistic understanding of sensory-guided behaviors.

Sweet neurons inhibit texture discrimination by signaling TMC-expressing mechanosensitive neurons in Drosophila

“…Second, although flies rely on mechanosensitive neurons on the labellum/proboscis to discriminate substrates of different hardness during feeding (Jeong et al, 2016; Zhang et al, 2016; Sánchez-Alcañiz et al, 2017b), the principal mechanosensitive neurons they use to discriminate hardness during egg-laying likely may be housed on the ovipositor instead since removal of none of the other appendages caused females unable to discriminate substrates of different hardness (Figure 2G). While we do not have direct evidence to support this claim, we note that ovipositor is known to possess mechanosensitive neurons (Sánchez-Alcañiz and Benton, 2017a; Stocker, 1994; Newland and Burrows, 1994) and that flies have been shown to actively probe substrates with their ovipositor prior to depositing each egg (Yang et al, 2008). Third and most curiously, labellum and legs may house mechanosensitive neurons whose input acts to inhibit – as opposed to promote – discrimination of substrates of different hardness during egg-laying, as severing these appendages enhanced discrimination of substrates of different hardness (Figure 2E–G).…”

“…We based this tentative model on the following reasons. First, ovipositor is known to possess mechanosensitive neurons (Sánchez-Alcañiz and Benton, 2017a; Stocker, 1994; Newland and Burrows, 1994); second, flies have been shown to actively probe the substrates with their ovipositor prior to depositing each egg (Yang et al, 2008); third and most importantly, animals that lacked the a significant portion of virtually all other appendages (e.g. labellum, tarsi, wings) but had intact ovipositor were still capable of discriminating substrates of different hardness.…”

“…In addition to detecting and discriminating stimuli of different modalities, animals frequently need to integrate information detected by different sensory systems (Stein et al, 1988; Sánchez-Alcañiz and Benton, 2017a). The demand for sensory integration is particularly pressing when animals must choose among options that differ along several independent dimensions (McFarland, 1977).…”

Molecular and cellular modulators for multisensory integration in C. elegans

“…The ability to integrate multiple types of sensory stimuli requires not only the responses across peripheral sensory areas, but also the signal processing in downstream network of interneurons [1, 3, 5–8, 110]. In C .…”

Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

“…Chemo-and mechanosensation not necessarily exclude each other, as integration on the level of the circuit, the sensory neuron, and even the receptor has been demonstrated. [60] In summary, the molecules, receptors, and neuronal circuits that convey information from the female reproductive tract to the central nervous system and trigger female copulation have not yet identified. We propose that seminal fluid molecules could act as pheromones and release female singing when they are sensed by neurons in the female reproductive tract.…”