A Neural Mechanism for Time-Window Separation Resolves Ambiguity of Adaptive Coding
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{"title"=>"A Neural Mechanism for Time-Window Separation Resolves Ambiguity of Adaptive Coding", "type"=>"journal", "authors"=>[{"first_name"=>"K. Jannis", "last_name"=>"Hildebrandt", "scopus_author_id"=>"6701493619"}, {"first_name"=>"Bernhard", "last_name"=>"Ronacher", "scopus_author_id"=>"7003733140"}, {"first_name"=>"R. Matthias", "last_name"=>"Hennig", "scopus_author_id"=>"7005302364"}, {"first_name"=>"Jan", "last_name"=>"Benda", "scopus_author_id"=>"7006249846"}], "year"=>2015, "source"=>"PLoS Biology", "identifiers"=>{"isbn"=>"1545-7885", "issn"=>"15457885", "pui"=>"603498595", "sgr"=>"84926371310", "pmid"=>"25761097", "scopus"=>"2-s2.0-84926371310", "doi"=>"10.1371/journal.pbio.1002096"}, "id"=>"d9bca660-a4f1-3970-9a74-5feed8b7b37d", "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.", "link"=>"http://www.mendeley.com/research/neural-mechanism-timewindow-separation-resolves-ambiguity-adaptive-coding", "reader_count"=>36, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Medicine and Dentistry"=>3, "Agricultural and Biological Sciences"=>15, "Neuroscience"=>9, "Design"=>1, "Physics and Astronomy"=>2, "Psychology"=>2, "Computer Science"=>2, "Linguistics"=>1, "Engineering"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>9}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Computer Science"=>{"Computer Science"=>2}, "Linguistics"=>{"Linguistics"=>1}}, "reader_count_by_country"=>{"United States"=>2, "United Kingdom"=>1, "Germany"=>3}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1945390"], "description"=>"<p>A: In grasshoppers, the ears are located on each side of the first abdominal segment. The first step of neural processing takes place in the metathoracic ganglion. B: Metathoracic auditory pathway of grasshoppers: sound is transduced in receptor neurons in the ear and information is carried to the metathoracic ganglion, where receptors synapse on local neurons (both gray). These connect to ascending neurons, which in turn transfer auditory information about sound pattern (red) and direction (blue) separately up to the brain. C: Mean response of six local neurons (TN1) to an amplitude-modulated (AM) sound (bottom panel). The upper panel shows the spike frequency elicited by the sound played back at two different levels (black and red). The middle panel shows the first 130 ms of the response in more detail; the shaded areas depict standard deviation. The lower panel is the average difference between the responses in the middle panel ([response to louder sound minus response to softer sound]/response to louder sound). D: Example of a measurement of a level-response curve adapted to a given background level in a TN1 neuron. Gray boxes indicate the examples in panels E and F. E: Onset responses to level steps relative to a background level (numbers at the bottom) are independent of different background levels (indicated by line color); the neurons were adapted to a mean level as shown in D. F: Adaptation of level-response curves of a TN1 neuron to different background levels of sound. The black line is the response curve when tested in silence (error bars: standard error of the mean [SEM]); the colored curves represent adapted response curves of the same cell after adaptation to different background levels (dotted vertical lines). G: Shift of the parameterized level-response curves as a function of the background sound for all recorded TN1 (left panel) and receptor cells (right panel). The dashed black line is the prediction of complete compensation of the background level by adaptation, the red line a fit of a straight line to the data. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s003\" target=\"_blank\">S1 Data</a> for data underlying panels C–F.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333200, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Emergence_of_level_invariance_along_the_pathway_/1333200", "title"=>"Emergence of level invariance along the pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945391"], "description"=>"<p>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 <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s004\" target=\"_blank\">S2 Data</a> for experimental data underlying panels A–C and <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s001\" target=\"_blank\">S1 Code</a> for the code used to generate the modeling results in B and C. w/o: without.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333201, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intrinsic_adaptation_of_the_central_ILD_coding_neuron_/1333201", "title"=>"Intrinsic adaptation of the central ILD coding neuron.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945408"], "description"=>"<p>A: Schematic drawing of the network architecture. Receptors and local neurons (gray) are subsumed under “periphery” (for more details, see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.g001\" target=\"_blank\">Fig. 1</a>). B: Optimal peripheral response curve for coding of pattern (left) or direction (ILD, right) of a sound. The shaded areas in the left panel represent the amplitude distributions at the ipsi-lateral (gray) and the contralateral (red) side of the animal for lateralized sound. The solid lines represent the optimal response curves of the output of the ipsi- and contra-lateral peripheral network for pattern coding. Different levels or directions demand different peripheral response curves. The shaded area in the right panel represents the distribution of all ILD the animal may experience, restricted by the physical constraints of the ears. Dashed line represents optimal outputs of the periphery for direction coding.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333218, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g006", "stats"=>{"downloads"=>4, "page_views"=>154, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conflicting_demands_of_localization_and_pattern_representation_on_peripheral_adaptation_/1333218", "title"=>"Conflicting demands of localization and pattern representation on peripheral adaptation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945394"], "description"=>"<p>A: Response of a pair of modeled direction coding central neurons to an artificial grasshopper song played back from three directions (indicated by line colors) and the difference between the responses of the ipsi- and contralateral ascending neuron (bottom panel). B: Same simulation, but with intrinsic adaptation added to the model of the ascending/central neurons. C: Decoding of the ILD from the responses as pictured in (A). Responses of the AN pair to combinations of ten directions (ILDs) and 33 mean levels were used and classified for decoding performance of ILDs. Left panel: all syllables of the song taken into account, right panel: only responses to the first syllable of the song were used for classification. D: Classification as in C but with adaptation added to the central neurons in the model. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s002\" target=\"_blank\">S2 Code</a> for the code ran to model the network responses and classification of these responses.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333204, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ILD_coding_improves_with_additional_intrinsic_adaptation_in_the_central_ascending_neurons_/1333204", "title"=>"ILD coding improves with additional intrinsic adaptation in the central, ascending neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945397"], "description"=>"<p>A: Response differences of the model central neuron pair for nine different ILDs played back at different mean levels. Each colored line depicts a single value of ILDs, ranging from 1 dB (light blue) to 9 dB (orange). Upper panel: only responses to first syllable taken into account. Lower panel: responses averaged over the duration of the entire song. Response differences were normalized to the largest response. B: Equivalent to (A), but with added adaptation current in the central neurons. In particular, when averaging over the complete response, ILDs are encoded invariantly with respect to the mean sound intensity (horizontal course of the curves). C: Dependence of classification success on different values of the adaptation time constant of the intrinsic adaptation current in the model. The dashed line indicates the value that best fitted the experimentally observed time course of intrinsic adaptation in AN2 as obtained by current injection (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.g002\" target=\"_blank\">Fig. 2A</a>). Percentage correct includes correct classification within ±1 dB of the presented ILD. D: Information content of the confusion matrices in dependence on the adaptation time constant. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s002\" target=\"_blank\">S2 Code</a> for the code used to model the network responses and classification of these responses.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333208, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Level_invariance_of_ILD_coding_and_relevance_of_time_course_of_adaptation_/1333208", "title"=>"Level invariance of ILD coding and relevance of time course of adaptation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945416", "https://ndownloader.figshare.com/files/1945417", "https://ndownloader.figshare.com/files/1945418", "https://ndownloader.figshare.com/files/1945419", "https://ndownloader.figshare.com/files/1945420", "https://ndownloader.figshare.com/files/1945421", "https://ndownloader.figshare.com/files/1945422", "https://ndownloader.figshare.com/files/1945423", "https://ndownloader.figshare.com/files/1945424", "https://ndownloader.figshare.com/files/1945425", "https://ndownloader.figshare.com/files/1945426", "https://ndownloader.figshare.com/files/1945427", "https://ndownloader.figshare.com/files/1945428"], "description"=>"<div><p>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.</p></div>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333226, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1002096.s001", "https://dx.doi.org/10.1371/journal.pbio.1002096.s002", "https://dx.doi.org/10.1371/journal.pbio.1002096.s003", "https://dx.doi.org/10.1371/journal.pbio.1002096.s004", "https://dx.doi.org/10.1371/journal.pbio.1002096.s005", "https://dx.doi.org/10.1371/journal.pbio.1002096.s006", "https://dx.doi.org/10.1371/journal.pbio.1002096.s007", "https://dx.doi.org/10.1371/journal.pbio.1002096.s008", "https://dx.doi.org/10.1371/journal.pbio.1002096.s009", "https://dx.doi.org/10.1371/journal.pbio.1002096.s010", "https://dx.doi.org/10.1371/journal.pbio.1002096.s011", "https://dx.doi.org/10.1371/journal.pbio.1002096.s012", "https://dx.doi.org/10.1371/journal.pbio.1002096.s013"], "stats"=>{"downloads"=>6, "page_views"=>35, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Neural_Mechanism_for_Time_Window_Separation_Resolves_Ambiguity_of_Adaptive_Coding_/1333226", "title"=>"A Neural Mechanism for Time-Window Separation Resolves Ambiguity of Adaptive Coding", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-03-11 03:25:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1945404"], "description"=>"<p>A: Arrangement of experiments with male grasshopper in the center between the two movable speakers. Right panel shows stimuli that were used in experiments presented in B and C. B: Control experiment with model song (P1 in both speakers). For the analysis, three types of behavioral responses were counted: turns to the left, turns to the right, and forward jumps. The figure contains only turns. Whenever right and left turns are short of 100%, the remaining reactions were jumps. Gray line: equal intensities at both speakers, simulating frontal stimulation. C: Same experiments as in B, but one of the speakers always had a preceding adaptor before the songs were presented (P2). Right and left stimulation was switched randomly during the experiments, plotted in reference to the adaptor stimulus. Dotted line: response of the model. D and E: Behavioral responses to ramped up (black) or down (red) songs. D: Percentage of turns towards louder side (right or left, switched randomly). Asterisks mark significance in a Wilcoxon’s matched pairs signed rank test; * <i>p</i> = 0.05, *** <i>p</i> = 0.001; E Percentage of forward jumps as a function of inter-aural level difference. Error bars show SEM. F: Overall responsiveness of the males to the four different sets of stimuli presented in B–E: control (B), forward masking (C), ramped down (D and E), and ramped up (D and E). See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s005\" target=\"_blank\">S3 Data</a> for behavioral data underlying panels A-C and <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002096#pbio.1002096.s002\" target=\"_blank\">S2 Code</a> for the network model.</p>", "links"=>[], "tags"=>["localization neurons", "intensity ranges", "degrades information", "neural adaptation", "amplitude modulations", "Neural Mechanism", "sound levels", "ambiguity", "adaptive coding", "pattern information", "experimental data", "neurophysiological data", "auditory pathway", "sound localization", "signal"], "article_id"=>1333214, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["K. Jannis Hildebrandt", "Bernhard Ronacher", "R. Matthias Hennig", "Jan Benda"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002096.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Behavioral_tests_support_model_predictions_/1333214", "title"=>"Behavioral tests support model predictions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-11 03:25:54"}

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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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