Temporal selectivity of identified auditory neurons in the cricket brain

Schildberger, Klaus

doi:10.1007/bf00612635

Cited by 271 publications

(238 citation statements)

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“…However, the sensitivity of the population of neurons in the AL increases even after exposure to a tone. Pulse repetition is a very important feature of auditory stimuli in many insects, and central neurons discriminating pulse repetition rates have been described in the cricket (40) and the locust (41). Neurons tuned to pulsed sound have also been described in the moth central nervous system (42)(43)(44) and might be responsible for the stronger effects at the AL level observed when preexposing male moths with a bat sound compared with a tone.…”

Section: Discussionmentioning

confidence: 99%

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Anton¹,

Evengaard

Barrozo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Modulation of sensitivity to sensory cues by experience is essential for animals to adapt to a changing environment. Sensitization and adaptation to signals of the same modality as a function of experience have been shown in many cases, and some of the neurobiological mechanisms underlying these processes have been described. However, the influence of sensory signals on the sensitivity of a different modality is largely unknown. In males of the noctuid moth, Spodoptera littoralis, the sensitivity to the femaleproduced sex pheromone increases 24 h after a brief preexposure with pheromone at the behavioral and central nervous level. Here we show that this effect is not confined to the same sensory modality: the sensitivity of olfactory neurons can also be modulated by exposure to a different sensory stimulus, i.e., a pulsed stimulus mimicking echolocating sounds from attacking insectivorous bats. We tested responses of preexposed male moths in a walking bioassay and recorded from neurons in the primary olfactory center, the antennal lobe. We show that brief exposure to a bat call, but not to a behaviorally irrelevant tone, increases the behavioral sensitivity of male moths to sex pheromone 24 h later in the same way as exposure to the sex pheromone itself. The observed behavioral modification is accompanied by an increase in the sensitivity of olfactory neurons in the antennal lobe. Our data provide thus evidence for cross-modal experience-dependent plasticity not only on the behavioral level, but also on the central nervous level, in an insect.bat sound | plant odor | sexual behavior | intracellular recording A nimals live in an ever-changing environment and must be able to adapt their behavior in response to highly varying sensory cues. One way to achieve such adaptive behavior is through plasticity of the nervous system, whereby modifications can be induced depending on sensory input. Previous studies have shown that exposure to environmental signals during development and in early adult life might influence the precise design and sensitivity of the targeted sensory system (1-3). The development of the peripheral and central visual, auditory, somatosensory, and olfactory systems in vertebrates has been shown to be highly influenced by experience (e.g., refs. 4-11) and regulated by neurogenesis and network remodeling with, for example, axon growth, the increase of the number of synaptic connections, and the strengthening of existing synapses (ref. 1 and references therein; ref. 12).Different strategies to achieve high sensitivity for abundant and/ or important signals have evolved. One way is limited attention, whereby an animal focuses on a specific sensory system, or even on a specific type of sensory signal, whereas other, simultaneously occurring information signals might be less attended (13,14). Experience of sensory input with a behaviorally important stimulus could also elicit long-term changes, which improve the insect's ability to respond to that specific stimulus (e.g., ref. 15). Furthermore, brief s...

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Section: Discussionmentioning

confidence: 99%

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Anton¹,

Evengaard

Barrozo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…We first compared the behavioral phonotactic responses with the spike activity of the ascending interneuron TH1-AC1, which is the only ascending interneuron forwarding calling-songspecific information from the prothoracic auditory neuropil toward the brain (Wohlers and Huber, 1982;Schildberger, 1984). The activity of this neuron has been described but never comprehensively compared against phonotactic tuning to different temporal paradigms.…”

Section: Temporal Selectivity Of Phonotaxis and Of The Ascending Intementioning

confidence: 99%

“…Further to these advances in lower vertebrates, the neural networks of insects provide the advantage to analyze and reveal principles of auditory processing at the level of identified neurons (Wohlers and Huber, 1982;Schildberger, 1984;Brodfuehrer and Hoy, 1990;Zorović and Hedwig, 2011). Phonotactic behavior of female crickets is tuned to the temporal structure of the male calling song.…”

Section: Introductionmentioning

confidence: 99%

“…Data from Bush and Schul (2006) indicate that temporal pattern recognition may be achieved by oscillatory responses of individual neurons. Based on intracellular recordings of auditory brain neurons, Schildberger (1984) suggested that temporal filtering is established by sequential processing in low-pass and high-pass filter neurons that finally shape the bandpass response properties of brain neurons that match the temporal tuning of female phonotaxis.…”

Section: Introductionmentioning

confidence: 99%

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Calling Song Recognition in Female Crickets: Temporal Tuning of Identified Brain Neurons Matches Behavior

Kostarakos¹,

Hedwig²

2012

Journal of Neuroscience

113

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Phonotactic orientation of female crickets is tuned to the temporal pattern of the male calling song. We analyzed the phonotactic selectivity of female crickets to varying temporal features of calling song patterns and compared it with the auditory response properties of the ascending interneuron AN1 (herein referred to as TH1-AC1) and four newly identified local brain neurons. The neurites of all brain neurons formed a ring-like branching pattern in the anterior protocerebrum that overlapped with the axonal arborizations of TH1-AC1. All brain neurons responded phasically to the sound pulses of a species-specific chirp. The spike activity of TH1-AC1 and the local interneuron, B-LI2, copied different auditory patterns regardless of their temporal structure. Two other neurons, B-LI3 and B-LC3, matched the temporal selectivity of the phonotactic responses but also responded to some nonattractive patterns. Neuron B-LC3 linked the bilateral auditory areas in the protocerebrum. One local brain neuron, B-LI4, received inhibitory as well as excitatory synaptic inputs. Inhibition was particularly pronounced for nonattractive pulse patterns, reducing its spike activity. When tested with different temporal patterns, B-LI4 exhibited bandpass response properties; its different auditory response functions significantly matched the tuning of phonotaxis. Temporal selectivity was established already for the second of two sound pulses separated by one species-specific pulse interval. Temporal pattern recognition in the cricket brain occurs within the anterior protocerebrum at the first stage of auditory processing. It is crucially linked to a change in auditory responsiveness during pulse intervals and based on fast interactions of inhibition and excitation.

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“…Neurons that show selectivity for temporal pattern exist in the central nervous systems of a variety of organisms (Rose 1986). Bandpass filter neurons that are tuned to the temporal pattern of calling song have been identified in the brain of the field cricket, Gryllus bimaculatus (Schildberger 1984). …”

Section: The Necessary Acoustic Parameters Of Courtship Songmentioning

confidence: 99%

Recognition of courtship song in the field cricket,Teleogryllus oceanicus

Balakrishnan

Pollack

1996

Animal Behaviour

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Abstract. The courtship song of the cricket, Teleogryllus oceanicus plays an important role in inducing the female to mount the male, which is necessary for mating. The song consists of a short, amplitude-modulated chirp, followed by a long trill of constant intensity and high syllable rate. Using playback techniques, it was determined which physical parameters of courtship song are necessary and/or sufficient to evoke normal female mounting of muted, courting males. The higher harmonics of natural courtship song were neither necessary nor sufficient for the effectiveness of the song. The chirp component alone was sufficient to evoke normal levels of mounting, but the trill was only partially effective on its own. The conspicuous amplitude modulation of the chirp was not necessary to evoke normal responses. The results suggest that the high effectiveness of the chirp is due to its characteristic temporal pattern. As in other cricket species, the song repertoire of T. oceanicus also includes distinct calling and aggression songs, which contain chirps that are structurally similar to the courtship chirp. Both calling and aggression songs evoked normal mounting responses when played back in the context of courtship.

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Temporal selectivity of identified auditory neurons in the cricket brain

Cited by 271 publications

References 27 publications

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Calling Song Recognition in Female Crickets: Temporal Tuning of Identified Brain Neurons Matches Behavior

Recognition of courtship song in the field cricket,Teleogryllus oceanicus

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