An official website of the United States government
Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered thatDrosophilaperform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on theDrosophilahead that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.
more »
« less
Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
Diverse mechanosensory neurons detect different mechanical forces that can impact animal behavior. Yet our understanding of the anatomical and physiological diversity of these neurons and the behaviors that they influence is limited. We previously discovered that grooming of the Drosophila melanogaster antennae is elicited by an antennal mechanosensory chordotonal organ, the Johnston’s organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations that each elicit antennal grooming. We show that the subpopulations project to different, discrete zones in the brain and differ in their responses to mechanical stimulation of the antennae. Although activation of each subpopulation elicits antennal grooming, distinct subpopulations also elicit the additional behaviors of wing flapping or backward locomotion. Our results provide a comprehensive description of the diversity of mechanosensory neurons in the JO, and reveal that distinct JO subpopulations can elicit both common and distinct behavioral responses.
more »
« less
- Award ID(s):
- 1736019
- PAR ID:
- 10288534
- Date Published:
- Journal Name:
- eLife
- Volume:
- 9
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
The Lim1 transcription factor is required in Drosophila for patterning the eye-antennal disk. At the adult stage, Lim1 is strongly expressed in Johnston’s Organ (JO) neurons, the antennal auditory organ. Using RNAi-mediated knockdown of Lim1 using a strong neuronal driver, we find a significant reduction in electrophysiological responses to auditory stimuli, recorded from the antennal nerve. This reduction can be accounted for by Lim1 knockdown in the auditory subset of JO neurons, with no effect of knockdown in JO neuron subsets associated with wind or gravity detection. Conversely, Lim1 knockdown in JO sense organ precursors had no effect on hearing. Mosaic animals with antennal clones of the Lim1E9 null mutation showed morphological defects in the antenna, and significant auditory electrophysiological defects. Our results are consistent with two distinct functions for Lim1 in the antenna, including an early patterning function in the eye-antennal disk, and a later neural differentiation function in the JO neurons.more » « less
-
In nature, olfactory signals are delivered to detectors—for example, insect antennae—by means of turbulent air, which exerts concurrent chemical and mechanical stimulation on the detectors. The antennal lobe, which is traditionally viewed as a chemosensory module, sits downstream of antennal inputs. We review experimental evidence showing that, in addition to being a chemosensory structure, antennal lobe neurons also respond to mechanosensory input in the form of wind speed. Benchmarked with empirical data, we constructed a dynamical model to simulate bimodal integration in the antennal lobe, with model dynamics yielding insights such as a positive correlation between the strength of mechanical input and the capacity to follow high frequency odor pulses, an important task in tracking odor sources. Furthermore, we combine experimental and theoretical results to develop a conceptual framework for viewing the functional significance of sensory integration within the antennal lobe. We formulate the testable hypothesis that the antennal lobe alternates between two distinct dynamical regimes, one which benefits odor plume tracking and one which promotes odor discrimination. We postulate that the strength of mechanical input, which correlates with behavioral contexts such being mid-flight versus hovering near a flower, triggers the transition from one regime to the other.more » « less
-
Skoulakis, Efthimios M. (Ed.)Animals are constantly bombarded with stimuli, which presents a fundamental problem of sorting among pervasive uninformative stimuli and novel, possibly meaningful stimuli. We evaluated novelty detection behaviorally in honey bees as they position their antennae differentially in an air stream carrying familiar or novel odors. We then characterized neuronal responses to familiar and novel odors in the first synaptic integration center in the brain–the antennal lobes. We found that the neurons that exhibited stronger initial responses to the odor that was to be familiarized are the same units that later distinguish familiar and novel odors, independently of chemical identities. These units, including both tentative projection neurons and local neurons, showed a decreased response to the familiar odor but an increased response to the novel odor. Our results suggest that the antennal lobe may represent familiarity or novelty to an odor stimulus in addition to its chemical identity code. Therefore, the mechanisms for novelty detection may be present in early sensory processing, either as a result of local synaptic interaction or via feedback from higher brain centers.more » « less
-
Wagner, William R (Ed.)To probe its environment, the flying insect controllably flexes, twists, and maneuvers its antennae by coupling mechanical deformations with the sensory output. We question how the materials properties of insect antennae could influence their performance. A comparative study was conducted on four hawkmoth species: Manduca sexta, Ceratomia catalpae, Manduca quinquemaculata, and Xylophanes tersa. The morphology of the antennae of three hawkmoths that hover while feeding and one putatively non-nectar-feeding hawkmoth (Ceratomia catalpa) do not fundamentally differ, and all the antennae are comb-like (i.e., pectinate), markedly in males but weakly in females. Applying different weights to the free end of extracted cantilevered antennae, we discovered anisotropy in flexural rigidity when the antenna is forced to bend dorsally versus ventrally. The flexural rigidity of male antennae was less than that of females. Compared with the hawkmoths that hover while feeding, Ceratomia catalpae has almost two orders of magnitude lower flexural rigidity. Tensile tests showed that the stiffness of male and female antennae is almost the same. Therefore, the differences in flexural rigidity are explained by the distinct shapes of the antennal pectination. Like bristles in a comb, the pectinations provide extra rigidity to the antenna. We discuss the biological implications of these discoveries in relation to the flight habits of hawkmoths. Flexural anisotropy of antennae is expected in other groups of insects, but the targeted outcome may differ. Our work offers promising new applications of shaped fibers as mechanical sensors.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.59976
