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A neural mechanism for time-window separation resolves ambiguity of adaptive coding.

Hildebrandt KJ, Ronacher B, Hennig RM, Benda J - PLoS Biol. (2015)

Bottom Line: Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it.We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally.In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

View Article: PubMed Central - PubMed

Affiliation: Cluster of Excellence "Hearing4all", Department for Neuroscience, University of Oldenburg, Oldenburg, Germany.

ABSTRACT
The senses of animals are confronted with changing environments and different contexts. Neural adaptation is one important tool to adjust sensitivity to varying intensity ranges. For instance, in a quiet night outdoors, our hearing is more sensitive than when we are confronted with the plurality of sounds in a large city during the day. However, adaptation also removes available information on absolute sound levels and may thus cause ambiguity. Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it. We present an example where adaptation is beneficial for one task--namely, the reliable encoding of the pattern of an acoustic signal-but detrimental for another--the localization of the same acoustic stimulus. With a combination of neurophysiological data, modeling, and behavioral tests, we show that adaptation in the periphery of the auditory pathway of grasshoppers enables intensity-invariant coding of amplitude modulations, but at the same time, degrades information available for sound localization. We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally. In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

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Intrinsic adaptation of the central ILD coding neuron.A: Response adaptation of an AN2 neuron to 500 ms current injection. B: The same neuron stimulated with a 500 ms sound stimulus of constant intensity level (56 dB SPL). The dotted line depicts responses of a model of AN2 that does not include the intrinsic adaptation seen in (A) but receives adapting inputs from the periphery (inset). C: Incorporation of an intrinsic adaptation current into the AN2 model reproduces the strong adaptation in response to acoustic stimuli. See S2 Data for experimental data underlying panels A–C and S1 Code for the code used to generate the modeling results in B and C. w/o: without.
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pbio.1002096.g002: Intrinsic adaptation of the central ILD coding neuron.A: Response adaptation of an AN2 neuron to 500 ms current injection. B: The same neuron stimulated with a 500 ms sound stimulus of constant intensity level (56 dB SPL). The dotted line depicts responses of a model of AN2 that does not include the intrinsic adaptation seen in (A) but receives adapting inputs from the periphery (inset). C: Incorporation of an intrinsic adaptation current into the AN2 model reproduces the strong adaptation in response to acoustic stimuli. See S2 Data for experimental data underlying panels A–C and S1 Code for the code used to generate the modeling results in B and C. w/o: without.

Mentions: In the grasshopper, direction is encoded in two pairs of ascending interneurons that each receives excitatory input from one side and inhibitory input from the other. In a previous study, we had observed a strong intrinsic activity-dependent adaptation current in one of these neurons (AN2) [29]. When current was injected into the AN2, spike frequency quickly dropped down to very low levels (Fig. 2A) and often completely disappeared at higher current levels. In response to sound stimuli the AN2 displayed an even stronger reduction in firing (Fig. 2B). Since an intrinsic adaptation mechanism restricts firing mostly to the onset of the stimulus that still contains information on absolute sound levels, we hypothesized that intrinsic adaptation could enable the coding of direction despite the observed peripheral adaptation.


A neural mechanism for time-window separation resolves ambiguity of adaptive coding.

Hildebrandt KJ, Ronacher B, Hennig RM, Benda J - PLoS Biol. (2015)

Intrinsic adaptation of the central ILD coding neuron.A: Response adaptation of an AN2 neuron to 500 ms current injection. B: The same neuron stimulated with a 500 ms sound stimulus of constant intensity level (56 dB SPL). The dotted line depicts responses of a model of AN2 that does not include the intrinsic adaptation seen in (A) but receives adapting inputs from the periphery (inset). C: Incorporation of an intrinsic adaptation current into the AN2 model reproduces the strong adaptation in response to acoustic stimuli. See S2 Data for experimental data underlying panels A–C and S1 Code for the code used to generate the modeling results in B and C. w/o: without.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4356587&req=5

pbio.1002096.g002: Intrinsic adaptation of the central ILD coding neuron.A: Response adaptation of an AN2 neuron to 500 ms current injection. B: The same neuron stimulated with a 500 ms sound stimulus of constant intensity level (56 dB SPL). The dotted line depicts responses of a model of AN2 that does not include the intrinsic adaptation seen in (A) but receives adapting inputs from the periphery (inset). C: Incorporation of an intrinsic adaptation current into the AN2 model reproduces the strong adaptation in response to acoustic stimuli. See S2 Data for experimental data underlying panels A–C and S1 Code for the code used to generate the modeling results in B and C. w/o: without.
Mentions: In the grasshopper, direction is encoded in two pairs of ascending interneurons that each receives excitatory input from one side and inhibitory input from the other. In a previous study, we had observed a strong intrinsic activity-dependent adaptation current in one of these neurons (AN2) [29]. When current was injected into the AN2, spike frequency quickly dropped down to very low levels (Fig. 2A) and often completely disappeared at higher current levels. In response to sound stimuli the AN2 displayed an even stronger reduction in firing (Fig. 2B). Since an intrinsic adaptation mechanism restricts firing mostly to the onset of the stimulus that still contains information on absolute sound levels, we hypothesized that intrinsic adaptation could enable the coding of direction despite the observed peripheral adaptation.

Bottom Line: Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it.We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally.In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

View Article: PubMed Central - PubMed

Affiliation: Cluster of Excellence "Hearing4all", Department for Neuroscience, University of Oldenburg, Oldenburg, Germany.

ABSTRACT
The senses of animals are confronted with changing environments and different contexts. Neural adaptation is one important tool to adjust sensitivity to varying intensity ranges. For instance, in a quiet night outdoors, our hearing is more sensitive than when we are confronted with the plurality of sounds in a large city during the day. However, adaptation also removes available information on absolute sound levels and may thus cause ambiguity. Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it. We present an example where adaptation is beneficial for one task--namely, the reliable encoding of the pattern of an acoustic signal-but detrimental for another--the localization of the same acoustic stimulus. With a combination of neurophysiological data, modeling, and behavioral tests, we show that adaptation in the periphery of the auditory pathway of grasshoppers enables intensity-invariant coding of amplitude modulations, but at the same time, degrades information available for sound localization. We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally. In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

Show MeSH