scholarly journals An arousal-gated visual circuit controls pursuit during Drosophila courtship

Author(s):  
Tom Hindmarsh Sten ◽  
Rufei Li ◽  
Adriane Otopalik ◽  
Vanessa Ruta

Long-lasting internal states, like hunger, aggression, and sexual arousal, pattern ongoing behavior by defining how the sensory world is translated to specific actions that subserve the needs of an animal. Yet how enduring internal states shape sensory processing or behavior has remained unclear. In Drosophila, male flies will perform a lengthy and elaborate courtship ritual, triggered by activation of sexually-dimorphic P1 neurons, in which they faithfully follow and sing to a female. Here, by recording from males as they actively court a fictive ‘female’ in a virtual environment, we gain insight into how the salience of female visual cues is transformed by a male’s internal arousal state to give rise to persistent courtship pursuit. We reveal that the gain of LCt0a visual projection neurons is strongly increased during courtship, enhancing their sensitivity to moving targets. A simple network model based on the LCt0a circuit accurately predicts a male’s tracking of a female over hundreds of seconds, underscoring that LCt0a visual signals, once released by P1-mediated arousal, become coupled to motor pathways to deterministically control his visual pursuit. Furthermore, we find that P1 neuron activity correlates with fluctuations in the intensity of a male’s pursuit, and that their acute activation is sufficient to boost the gain of the LCt0 pathways. Together, these results reveal how alterations in a male’s internal arousal state can dynamically modulate the propagation of visual signals through a high-fidelity visuomotor circuit to guide his moment-to-moment performance of courtship.

Author(s):  
Ming Wu ◽  
Aljoscha Nern ◽  
W Ryan Williamson ◽  
Mai M Morimoto ◽  
Michael B Reiser ◽  
...  

2000 ◽  
Vol 203 (11) ◽  
pp. 1701-1709 ◽  
Author(s):  
P. Kloppenburg ◽  
T. Heinbockel

Extra- and intracellular recordings from an intact brain preparation were used to study the effects of 5-hydroxytryptamine (5-HT or serotonin) on projection neurons in the sexually dimorphic macroglomerular complex (MGC) in the antennal lobe of the male moth Manduca sexta. The MGC is a group of three identified glomeruli specialized for synaptic processing of primary afferent information about the multi-component sex pheromone of the female. We investigated the modulatory effects of 5-HT on pheromone-evoked local field potentials in the MGC. The magnitude and duration of these potentials, which are thought to be generated by a population of pheromone-sensitive projection neurons of the MGC, were increased by 5-HT. Using intracellular recordings from the neurites of individual MGC projection neurons, we found that 5-HT increased the number of action potentials in response to pheromonal stimulation. These findings correlate well with earlier experiments that used other recording techniques. Our results are further evidence that 5-HT modulates a population of pheromone-sensitive MGC projection neurons that relay information about the pheromonal stimulus from the MGC to higher-order centers in the protocerebrum and are therefore pivotal for mate-finding and odor-guided behavior.


2014 ◽  
Vol 281 (1785) ◽  
pp. 20133201 ◽  
Author(s):  
Federico Rossano ◽  
Marie Nitzschner ◽  
Michael Tomasello

Domestic dogs are particularly skilled at using human visual signals to locate hidden food. This is, to our knowledge, the first series of studies that investigates the ability of dogs to use only auditory communicative acts to locate hidden food. In a first study, from behind a barrier, a human expressed excitement towards a baited box on either the right or left side, while sitting closer to the unbaited box. Dogs were successful in following the human's voice direction and locating the food. In the two following control studies, we excluded the possibility that dogs could locate the box containing food just by relying on smell, and we showed that they would interpret a human's voice direction in a referential manner only when they could locate a possible referent (i.e. one of the boxes) in the environment. Finally, in a fourth study, we tested 8–14-week-old puppies in the main experimental test and found that those with a reasonable amount of human experience performed overall even better than the adult dogs. These results suggest that domestic dogs’ skills in comprehending human communication are not based on visual cues alone, but are instead multi-modal and highly flexible. Moreover, the similarity between young and adult dogs’ performances has important implications for the domestication hypothesis.


2006 ◽  
Vol 95 (6) ◽  
pp. 3596-3616 ◽  
Author(s):  
Eiji Hoshi ◽  
Jun Tanji

We examined neuronal activity in the dorsal and ventral premotor cortex (PMd and PMv, respectively) to explore the role of each motor area in processing visual signals for action planning. We recorded neuronal activity while monkeys performed a behavioral task during which two visual instruction cues were given successively with an intervening delay. One cue instructed the location of the target to be reached, and the other indicated which arm was to be used. We found that the properties of neuronal activity in the PMd and PMv differed in many respects. After the first cue was given, PMv neuron response mostly reflected the spatial position of the visual cue. In contrast, PMd neuron response also reflected what the visual cue instructed, such as which arm to be used or which target to be reached. After the second cue was given, PMv neurons initially responded to the cue's visuospatial features and later reflected what the two visual cues instructed, progressively increasing information about the target location. In contrast, the activity of the majority of PMd neurons responded to the second cue with activity reflecting a combination of information supplied by the first and second cues. Such activity, already reflecting a forthcoming action, appeared with short latencies (<400 ms) and persisted throughout the delay period. In addition, both the PMv and PMd showed bilateral representation on visuospatial information and motor-target or effector information. These results further elucidate the functional specialization of the PMd and PMv during the processing of visual information for action planning.


2013 ◽  
Vol 550 ◽  
pp. 156-161 ◽  
Author(s):  
Ying Yan ◽  
Ye Xu ◽  
Shengwen Deng ◽  
Naya Huang ◽  
Ying Yang ◽  
...  

2015 ◽  
Vol 114 (1) ◽  
pp. 284-300 ◽  
Author(s):  
Tianhe C. Zhang ◽  
John J. Janik ◽  
Ryan V. Peters ◽  
Gang Chen ◽  
Ru-Rong Ji ◽  
...  

Spinal cord stimulation (SCS) is a therapy used to treat intractable pain with a putative mechanism of action based on the Gate Control Theory. We hypothesized that sensory projection neuron responses to SCS would follow a single stereotyped response curve as a function of SCS frequency, as predicted by the Gate Control circuit. We recorded the responses of antidromically identified sensory projection neurons in the lumbar spinal cord during 1- to 150-Hz SCS in both healthy rats and neuropathic rats following chronic constriction injury (CCI). The relationship between SCS frequency and projection neuron activity predicted by the Gate Control circuit accounted for a subset of neuronal responses to SCS but could not account for the full range of observed responses. Heterogeneous responses were classifiable into three additional groups and were reproduced using computational models of spinal microcircuits representing other interactions between nociceptive and nonnociceptive sensory inputs. Intrathecal administration of bicuculline, a GABAA receptor antagonist, increased spontaneous and evoked activity in projection neurons, enhanced excitatory responses to SCS, and reduced inhibitory responses to SCS, suggesting that GABAA neurotransmission plays a broad role in regulating projection neuron activity. These in vivo and computational results challenge the Gate Control Theory as the only mechanism underlying SCS and refine our understanding of the effects of SCS on spinal sensory neurons within the framework of contemporary understanding of dorsal horn circuitry.


Author(s):  
Lorin Timaeus ◽  
Laura Geid ◽  
Gizem Sancer ◽  
Mathias F. Wernet ◽  
Thomas Hummel

SummaryOne hallmark of the visual system is the strict retinotopic organization from the periphery towards the central brain, spanning multiple layers of synaptic integration. Recent Drosophila studies on the computation of distinct visual features have shown that retinotopic representation is often lost beyond the optic lobes, due to convergence of columnar neuron types onto optic glomeruli. Nevertheless, functional imaging revealed a spatially accurate representation of visual cues in the central complex (CX), raising the question how this is implemented on a circuit level. By characterizing the afferents to a specific visual glomerulus, the anterior optic tubercle (AOTU), we discovered a spatial segregation of topographic versus non-topographic projections from molecularly distinct classes of medulla projection neurons (medullo-tubercular, or MeTu neurons). Distinct classes of topographic versus non-topographic MeTus form parallel channels, terminating in separate AOTU domains. Both types then synapse onto separate matching topographic fields of tubercular-bulbar (TuBu) neurons which relay visual information towards the dendritic fields of central complex ring neurons in the bulb neuropil, where distinct bulb sectors correspond to a distinct ring domain in the ellipsoid body. Hence, peripheral topography is maintained due to stereotypic circuitry within each TuBu class, providing the structural basis for spatial representation of visual information in the central complex. Together with previous data showing rough topography of lobula projections to a different AOTU subunit, our results further highlight the AOTUs role as a prominent relay station for spatial information from the retina to the central brain.


2019 ◽  
Author(s):  
Ross M McKinney ◽  
Yehuda Ben-Shahar

SummaryLike other mating behaviors, the courtship ritual exhibited by male Drosophila towards a virgin female is comprised of spatiotemporal sequences of innate behavioral elements. Yet, the specific stimuli and neural circuits that determine when and where males release individual courtship elements are not well understood. Here, we investigated the role of visual object recognition in the release of specific behavioral elements during bouts of male courtship. By using a computer vision and machine learning based approach for high-resolution analyses of the male courtship ritual, we show that the release of distinct behavioral elements occur at stereotyped locations around the female and depends on the ability of males to recognize visual landmarks present on the female. Specifically, we show that independent of female motion, males utilize unique populations of visual projection neurons to recognize the eyes of a target female, which is essential for the release of courtship behaviors at their appropriate spatial locations. Together, these results provide a mechanistic explanation for how relatively simple visual cues could play a role in driving both spatially- and temporally-complex social interactions.


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