scholarly journals Quadratic and adaptive computations yield an efficient representation of song in Drosophila auditory receptor neurons

2021 ◽  
Author(s):  
Jan Clemens ◽  
Mala Murthy

Sensory neurons encode information using multiple nonlinear and dynamical transformations. For instance, auditory receptor neurons in Drosophila adapt to the mean and the intensity of the stimulus, change their frequency tuning with sound intensity, and employ a quadratic nonlinearity. While these computations are considered advantageous in isolation, their combination can lead to a highly ambiguous and complex code that is hard to decode. Combining electrophysiological recordings and computational modelling, we investigate how the different computations found in auditory receptor neurons in Drosophila combine to encode behaviorally-relevant acoustic signals like the courtship song. The computational model consists of a quadratic filter followed by a divisive normalization stage and reproduces population neural responses to artificial and natural sounds. For general classes of sounds, like band-limited noise, the representation resulting from these highly nonlinear computations is highly ambiguous and does not allow for a recovery of information about the frequency content and amplitude pattern. However, for courtship song, the code is simple and efficient: The quadratic filter improves the representation of the song envelope while preserving information about the song's fine structure across intensities. Divisive normalization renders the presentation of the song envelope robust to the relatively slow fluctuations in intensity that arise during social interactions, while preserving information about the species-specific fast fluctuations of the envelope. Overall, we demonstrate how a sensory system can benefit from adaptive and nonlinear computations while minimizing concomitant costs arising from ambiguity and complexity of readouts by adapting the code for behaviorally-relevant signals.

2019 ◽  
Author(s):  
Holger R. Goerlitz ◽  
Hannah M. ter Hofstede ◽  
Marc W. Holderied

AbstractMost animals are at risk from multiple predators and can vary anti-predator behaviour based on the level of threat posed by each predator. Animals use sensory systems to detect predator cues, but the relationship between the tuning of sensory systems and the sensory cues related to predator threat are not well-studied at the community level. Noctuid moths have ultrasound-sensitive ears to detect the echolocation calls of predatory bats. Here, combining empirical data and mathematical modelling, we show that moth hearing is adapted to provide information about the threat posed by different sympatric bat species. First, we found that multiple characteristics related to the threat posed by bats to moths correlate with bat echolocation call frequency. Second, the frequency tuning of the most sensitive auditory receptor in noctuid moth ears provides information allowing moths to escape detection by all sympatric bats with similar safety margin distances. Third, the least sensitive auditory receptor usually responds to bat echolocation calls at a similar distance across all moth species for a given bat species. If this neuron triggers last-ditch evasive flight, it suggests that there is an ideal reaction distance for each bat species, regardless of moth size. This study shows that even a very simple sensory system can adapt to deliver information suitable for triggering appropriate defensive reactions to each predator in a multiple predator community.


2001 ◽  
Vol 21 (9) ◽  
pp. 3215-3227 ◽  
Author(s):  
Christian K. Machens ◽  
Martin B. Stemmler ◽  
Petra Prinz ◽  
Rüdiger Krahe ◽  
Bernhard Ronacher ◽  
...  

2021 ◽  
Vol 12 ◽  
Author(s):  
Habibe K. Üçpunar ◽  
Ilona C. Grunwald Kadow

CO2 differs from most other odors by being ubiquitously present in the air animals inhale. CO2 levels of the atmosphere, however, are subject to change. Depending on the landscape, temperature, and time of the year, CO2 levels can change even on shortest time scales. In addition, since the 18th century the CO2 baseline keeps increasing due to the intensive fossil fuel usage. However, we do not know whether this change is significant for animals, and if yes whether and how animals adapt to this change. Most insects possess olfactory receptors to detect the gaseous molecule, and CO2 is one of the key odorants for insects such as the vinegar fly Drosophila melanogaster to find food sources and to warn con-specifics. So far, CO2 and its sensory system have been studied in the context of rotting fruit and other CO2-emitting sources to investigate flies’ response to significantly elevated levels of CO2. However, it has not been addressed whether flies detect and potentially react to atmospheric levels of CO2. By using behavioral experiments, here we show that flies can detect atmospheric CO2 concentrations and, if given the choice, prefer air with sub-atmospheric levels of the molecule. Blocking the synaptic release from CO2 receptor neurons abolishes this choice. Based on electrophysiological recordings, we hypothesize that CO2 receptors, similar to ambient temperature receptors, actively sample environmental CO2 concentrations close to atmospheric levels. Based on recent findings and our data, we hypothesize that Gr-dependent CO2 receptors do not primarily serve as a cue detector to find food sources or avoid danger, instead they function as sensors for preferred environmental conditions.


2010 ◽  
Vol 103 (3) ◽  
pp. 1614-1621 ◽  
Author(s):  
Patrick Sabourin ◽  
Gerald S. Pollack

Auditory receptor neurons of crickets are most sensitive to either low or high sound frequencies. Earlier work showed that the temporal coding properties of first-order auditory interneurons are matched to the temporal characteristics of natural low- and high-frequency stimuli (cricket songs and bat echolocation calls, respectively). We studied the temporal coding properties of receptor neurons and used modeling to investigate how activity within populations of low- and high-frequency receptors might contribute to the coding properties of interneurons. We confirm earlier findings that individual low-frequency-tuned receptors code stimulus temporal pattern poorly, but show that coding performance of a receptor population increases markedly with population size, due in part to low redundancy among the spike trains of different receptors. By contrast, individual high-frequency-tuned receptors code a stimulus temporal pattern fairly well and, because their spike trains are redundant, there is only a slight increase in coding performance with population size. The coding properties of low- and high-frequency receptor populations resemble those of interneurons in response to low- and high-frequency stimuli, suggesting that coding at the interneuron level is partly determined by the nature and organization of afferent input. Consistent with this, the sound-frequency-specific coding properties of an interneuron, previously demonstrated by analyzing its spike train, are also apparent in the subthreshold fluctuations in membrane potential that are generated by synaptic input from receptor neurons.


2010 ◽  
Vol 104 (3) ◽  
pp. 1219-1229 ◽  
Author(s):  
A. J. Hudspeth ◽  
Frank Jülicher ◽  
Pascal Martin

The sense of hearing achieves its striking sensitivity, frequency selectivity, and dynamic range through an active process mediated by the inner ear's mechanoreceptive hair cells. Although the active process renders hearing highly nonlinear and produces a wealth of complex behaviors, these various characteristics may be understood as consequences of a simple phenomenon: the Hopf bifurcation. Any critical oscillator operating near this dynamic instability manifests the properties demonstrated for hearing: amplification with a specific form of compressive nonlinearity and frequency tuning whose sharpness depends on the degree of amplification. Critical oscillation also explains spontaneous otoacoustic emissions as well as the spectrum and level dependence of the ear's distortion products. Although this has not been realized, several valuable theories of cochlear function have achieved their success by incorporating critical oscillators.


2013 ◽  
Vol 2013 ◽  
pp. 1-6 ◽  
Author(s):  
Danke Zhang ◽  
Yuanqing Li ◽  
Si Wu

The present study investigates a network model for implementing concentration-invariant representation for odors in the olfactory system. The network consists of olfactory receptor neurons, projection neurons, and inhibitory local neurons. Receptor neurons send excitatory inputs to projection neurons, which are modulated by the inhibitory inputs from local neurons. The modulation occurs at the presynaptic site from a receptor neuron to a projection one, leading to the operation of divisive normalization. The responses of local interneurons are determined by the total activities of olfactory receptor neurons. We find that with a proper parameter condition, the responses of projection neurons become effectively independent of the odor concentration. Simulation results confirm our theoretical analysis.


eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Frederic A Roemschied ◽  
Monika JB Eberhard ◽  
Jan-Hendrik Schleimer ◽  
Bernhard Ronacher ◽  
Susanne Schreiber

Changes in temperature affect biochemical reaction rates and, consequently, neural processing. The nervous systems of poikilothermic animals must have evolved mechanisms enabling them to retain their functionality under varying temperatures. Auditory receptor neurons of grasshoppers respond to sound in a surprisingly temperature-compensated manner: firing rates depend moderately on temperature, with average Q10 values around 1.5. Analysis of conductance-based neuron models reveals that temperature compensation of spike generation can be achieved solely relying on cell-intrinsic processes and despite a strong dependence of ion conductances on temperature. Remarkably, this type of temperature compensation need not come at an additional metabolic cost of spike generation. Firing rate-based information transfer is likely to increase with temperature and we derive predictions for an optimal temperature dependence of the tympanal transduction process fostering temperature compensation. The example of auditory receptor neurons demonstrates how neurons may exploit single-cell mechanisms to cope with multiple constraints in parallel.


2000 ◽  
Vol 203 (17) ◽  
pp. 2529-2537 ◽  
Author(s):  
V. Givois ◽  
G.S. Pollack

Auditory receptor neurons exhibit sensory habituation; their responses decline with repeated stimulation. We studied the effects of sensory habituation on the neural encoding of sound localization cues using crickets as a model system. In crickets, Teleogryllus oceanicus, sound localization is based on binaural comparison of stimulus intensity. There are two potential codes at the receptor-neuron level for interaural intensity difference: interaural difference in response strength, i.e. spike rate and/or count, and interaural difference in response latency. These are affected differently by sensory habituation. When crickets are stimulated with cricket-song-like trains of sound pulses, response strength declines for successive pulses in the train, and the decrease becomes more pronounced as the stimulus intensity increases. Response decrement is thus greater for receptors serving the ear ipsilateral to the sound source, where intensity is higher, resulting in a decrease in the interaural difference in response strength. Sensory habituation also affects response latency, which increases for responses to successive sound pulses in the stimulus train. The change in latency is independent of intensity, and thus is similar for receptors serving both ears. As a result, interaural latency difference is unaffected by sensory habituation and may be a more reliable cue for sound localization.


2006 ◽  
Vol 54 (1) ◽  
pp. 51 ◽  
Author(s):  
James H. Fullard

The ears of Oenosandra boisduvalii (Oenosandridae), as a representative of this heretofore unstudied family of moths, were electrophysiologically examined from specimens captured in South Australia. Male and female moths possess ears with two auditory receptor neurons that are similarly sensitive and tuned to the frequencies emitted by sympatric bats, suggesting that both sexes face equal predation pressures from aerially foraging bats. The two-celled ear of this moth supports the independence of the Oenosandridae from its previous affiliation with the Notodontidae, whose single auditory neuron remains a unique character within the Noctuoidea. The general insensitivity of its ear, however, resembles that of the notodontid moth and is surprising considering the diversity of insectivorous bats that forms its predation potential.


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