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Probing real sensory worlds of receivers with unsupervised clustering.

Pfeiffer M, Hartbauer M, Lang AB, Maass W, Römer H - PLoS ONE (2012)

Bottom Line: Our results show that the reliability of burst coding in the time domain is so high that identical stimuli lead to extremely similar spike pattern responses, even for different preparations on different dates, and even if one of the preparations is recorded outdoors and the other one in the sound proof lab.Our study shows that burst coding can provide a reliable mechanism for acoustic insects to classify and discriminate signals under very noisy real-world conditions.This gives new insights into the neural mechanisms potentially used by bushcrickets to discriminate conspecific songs from sounds of predators in similar carrier frequency bands.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Computer Science, TU Graz, Graz, Austria. pfeiffer@ini.phys.ethz.ch

ABSTRACT
The task of an organism to extract information about the external environment from sensory signals is based entirely on the analysis of ongoing afferent spike activity provided by the sense organs. We investigate the processing of auditory stimuli by an acoustic interneuron of insects. In contrast to most previous work we do this by using stimuli and neurophysiological recordings directly in the nocturnal tropical rainforest, where the insect communicates. Different from typical recordings in sound proof laboratories, strong environmental noise from multiple sound sources interferes with the perception of acoustic signals in these realistic scenarios. We apply a recently developed unsupervised machine learning algorithm based on probabilistic inference to find frequently occurring firing patterns in the response of the acoustic interneuron. We can thus ask how much information the central nervous system of the receiver can extract from bursts without ever being told which type and which variants of bursts are characteristic for particular stimuli. Our results show that the reliability of burst coding in the time domain is so high that identical stimuli lead to extremely similar spike pattern responses, even for different preparations on different dates, and even if one of the preparations is recorded outdoors and the other one in the sound proof lab. Simultaneous recordings in two preparations exposed to the same acoustic environment reveal that characteristics of burst patterns are largely preserved among individuals of the same species. Our study shows that burst coding can provide a reliable mechanism for acoustic insects to classify and discriminate signals under very noisy real-world conditions. This gives new insights into the neural mechanisms potentially used by bushcrickets to discriminate conspecific songs from sounds of predators in similar carrier frequency bands.

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Experimental arrangement for long-term recordings of single cell activity in the tropical rainforest.A) Illustration of the experimental arrangement. The inset shows the morphology of the cell within the prothoracic ganglion after intracellular dye injection (upper part), and a prototype of the portable preparation. B) Illustration of the five stimulus classes played to bushcrickets during experiments. 1) Single pulse of 10 ms; 2) double pulse with 10 ms duration each, separated by an interval of 10 ms; 3) 30 ms pulse; 4) four repetitive pulses, 10 ms each, separated by an interval of 10 ms; 5) 70 ms pulse. C, D) Examples of recordings made at about one hour before sunset (C), and 45 minutes after sunset (D), when the background noise level had increased from 40 dB SPL to 65 dB SPL. Note that in the low noise situation only a stimulus (arrow) elicited a short burst of spikes, whereas after sunset the neuron fires many bursts also in response to the acoustic background.
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pone-0037354-g001: Experimental arrangement for long-term recordings of single cell activity in the tropical rainforest.A) Illustration of the experimental arrangement. The inset shows the morphology of the cell within the prothoracic ganglion after intracellular dye injection (upper part), and a prototype of the portable preparation. B) Illustration of the five stimulus classes played to bushcrickets during experiments. 1) Single pulse of 10 ms; 2) double pulse with 10 ms duration each, separated by an interval of 10 ms; 3) 30 ms pulse; 4) four repetitive pulses, 10 ms each, separated by an interval of 10 ms; 5) 70 ms pulse. C, D) Examples of recordings made at about one hour before sunset (C), and 45 minutes after sunset (D), when the background noise level had increased from 40 dB SPL to 65 dB SPL. Note that in the low noise situation only a stimulus (arrow) elicited a short burst of spikes, whereas after sunset the neuron fires many bursts also in response to the acoustic background.

Mentions: A total of 27 adult male and female bushcrickets (Docidocercus gigliotosi) were used for this study. We recorded the activity of an identified auditory interneuron, the so-called omega neuron, in the field, using a technique introduced in [20] and [22], and explained in more detail in the Materials and Methods section. The morphology of the cell, as revealed from intracellular dye injection, is shown in Figure 1A (inset). It is a local neuron in the prothoracic ganglion and receives excitatory input from almost all of the 20–40 receptors in the hearing organ [23]. The tuning of the cell reflects the broad-band hearing sensitivity of the insect, matching both the frequencies of the conspecific calling song, and ultrasonic frequencies up to 100 kHz, thus including bat echolocation calls as well. As in other bushcricket species, the sensitivity of auditory receptors in D. gigliotosi differs by only a few dB from the sensitivity of the omega cell at most frequencies except below 5 kHz [24]. Furthermore, in response to a stimulus above its threshold, the neuron fires bursts of action potentials and copies the temporal pattern of an acoustic stimulus in a tonic manner. Altogether these attributes make outdoor recordings of the activity of the omega cell very suitable for studying sensory coding under realistic, i.e. outdoor conditions in the animals’ own natural habitat.


Probing real sensory worlds of receivers with unsupervised clustering.

Pfeiffer M, Hartbauer M, Lang AB, Maass W, Römer H - PLoS ONE (2012)

Experimental arrangement for long-term recordings of single cell activity in the tropical rainforest.A) Illustration of the experimental arrangement. The inset shows the morphology of the cell within the prothoracic ganglion after intracellular dye injection (upper part), and a prototype of the portable preparation. B) Illustration of the five stimulus classes played to bushcrickets during experiments. 1) Single pulse of 10 ms; 2) double pulse with 10 ms duration each, separated by an interval of 10 ms; 3) 30 ms pulse; 4) four repetitive pulses, 10 ms each, separated by an interval of 10 ms; 5) 70 ms pulse. C, D) Examples of recordings made at about one hour before sunset (C), and 45 minutes after sunset (D), when the background noise level had increased from 40 dB SPL to 65 dB SPL. Note that in the low noise situation only a stimulus (arrow) elicited a short burst of spikes, whereas after sunset the neuron fires many bursts also in response to the acoustic background.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368931&req=5

pone-0037354-g001: Experimental arrangement for long-term recordings of single cell activity in the tropical rainforest.A) Illustration of the experimental arrangement. The inset shows the morphology of the cell within the prothoracic ganglion after intracellular dye injection (upper part), and a prototype of the portable preparation. B) Illustration of the five stimulus classes played to bushcrickets during experiments. 1) Single pulse of 10 ms; 2) double pulse with 10 ms duration each, separated by an interval of 10 ms; 3) 30 ms pulse; 4) four repetitive pulses, 10 ms each, separated by an interval of 10 ms; 5) 70 ms pulse. C, D) Examples of recordings made at about one hour before sunset (C), and 45 minutes after sunset (D), when the background noise level had increased from 40 dB SPL to 65 dB SPL. Note that in the low noise situation only a stimulus (arrow) elicited a short burst of spikes, whereas after sunset the neuron fires many bursts also in response to the acoustic background.
Mentions: A total of 27 adult male and female bushcrickets (Docidocercus gigliotosi) were used for this study. We recorded the activity of an identified auditory interneuron, the so-called omega neuron, in the field, using a technique introduced in [20] and [22], and explained in more detail in the Materials and Methods section. The morphology of the cell, as revealed from intracellular dye injection, is shown in Figure 1A (inset). It is a local neuron in the prothoracic ganglion and receives excitatory input from almost all of the 20–40 receptors in the hearing organ [23]. The tuning of the cell reflects the broad-band hearing sensitivity of the insect, matching both the frequencies of the conspecific calling song, and ultrasonic frequencies up to 100 kHz, thus including bat echolocation calls as well. As in other bushcricket species, the sensitivity of auditory receptors in D. gigliotosi differs by only a few dB from the sensitivity of the omega cell at most frequencies except below 5 kHz [24]. Furthermore, in response to a stimulus above its threshold, the neuron fires bursts of action potentials and copies the temporal pattern of an acoustic stimulus in a tonic manner. Altogether these attributes make outdoor recordings of the activity of the omega cell very suitable for studying sensory coding under realistic, i.e. outdoor conditions in the animals’ own natural habitat.

Bottom Line: Our results show that the reliability of burst coding in the time domain is so high that identical stimuli lead to extremely similar spike pattern responses, even for different preparations on different dates, and even if one of the preparations is recorded outdoors and the other one in the sound proof lab.Our study shows that burst coding can provide a reliable mechanism for acoustic insects to classify and discriminate signals under very noisy real-world conditions.This gives new insights into the neural mechanisms potentially used by bushcrickets to discriminate conspecific songs from sounds of predators in similar carrier frequency bands.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Computer Science, TU Graz, Graz, Austria. pfeiffer@ini.phys.ethz.ch

ABSTRACT
The task of an organism to extract information about the external environment from sensory signals is based entirely on the analysis of ongoing afferent spike activity provided by the sense organs. We investigate the processing of auditory stimuli by an acoustic interneuron of insects. In contrast to most previous work we do this by using stimuli and neurophysiological recordings directly in the nocturnal tropical rainforest, where the insect communicates. Different from typical recordings in sound proof laboratories, strong environmental noise from multiple sound sources interferes with the perception of acoustic signals in these realistic scenarios. We apply a recently developed unsupervised machine learning algorithm based on probabilistic inference to find frequently occurring firing patterns in the response of the acoustic interneuron. We can thus ask how much information the central nervous system of the receiver can extract from bursts without ever being told which type and which variants of bursts are characteristic for particular stimuli. Our results show that the reliability of burst coding in the time domain is so high that identical stimuli lead to extremely similar spike pattern responses, even for different preparations on different dates, and even if one of the preparations is recorded outdoors and the other one in the sound proof lab. Simultaneous recordings in two preparations exposed to the same acoustic environment reveal that characteristics of burst patterns are largely preserved among individuals of the same species. Our study shows that burst coding can provide a reliable mechanism for acoustic insects to classify and discriminate signals under very noisy real-world conditions. This gives new insights into the neural mechanisms potentially used by bushcrickets to discriminate conspecific songs from sounds of predators in similar carrier frequency bands.

Show MeSH
Related in: MedlinePlus