Learning to Encode Timing: Mechanisms of Plasticity in the Auditory Brainstem — TEI-tagged view

Thanos Tzounopoulos, Nina Kraus · 2009 · neuroscience · doi:10.1016/j.neuron.2009.05.002 · full text at the source · TEI xml · tagged edition · index · concepts · authors
Where this record's text came from. faceted 2026-08 by reading the locally held text (xml); every evidence string verified as an exact substring of that text before merging. This is a Neuron review, so 'method' is review and the limitations quoted are limits of the evidence base it surveys rather than of an experiment the authors ran — the article states no limits on its own procedure. Claim type is existence (plasticity does occur in the brainstem); the same sentences also function as a critique of the traditional hard-wired view, but that view is never attributed to a named source, so no contradicts relation was recorded. Only one claim_relation qualifies: the Reverse Hierarchy Theory is named in the text ("A theory to account for the interactions between sensory input and top-down processes (e.g., attention, language, and memory) is the Reverse Hierarchy Theory (RHT) ( Ahissar and Hochstein, 2004 ).") and the authors explicitly propose extending it subcortically. Authors field is empty in the queue metadata and the text below the line does not name them. 2026-08-12 and 2026-08-15 schema-0.3 passes: every quote verified as an exact substring of the staged text and anchored at merge time; concept terms verified present; every edge endpoint an existing node.
This record’s own method is review, and the tags below follow from that. A review’s findings, quantities and statistics are things stated IN this paper, and some of them report results obtained elsewhere. No tag on this page names a different author. Measured across every review in this corpus, 81% of a review’s tags carry no citation at all — most of them are the review speaking. The corpus does not adjudicate the rest: read an unmarked tag as a claim this paper makes, not necessarily one it made first.
Other fields define these differently the same word, defined another way in another discipline
plasticity 4 fields
Tags on this paper every tag the record carries, whether or not the words occur in the text below — a number is how many papers in the corpus carry that tag; a tag with no number is unique to this paper
auditory brainstem plasticity11 intrinsic plasticity2 spike-timing-dependent plasticity Hebbian2 anti-Hebbian long-term potentiation2 long-term depression2 dorsal cochlear nucleus2 fusiform cartwheel cells medial nucleus of the trapezoid body auditory brainstem response frequency following response phase locking4 pitch tracking interaural time differences Reverse Hierarchy Theory corticofugal2 tinnitus4 Kv3.1b negative image musicians review319

Our tag layer for this paper

Cross-disciplinary analysis
content-tags & facets: phenomenon · claim-type · cross-domain-transfer · mechanism · claim-relation · replication-status · limitation — grounded in the full text
phenomenonauditory brainstem plasticity— “In agreement with activity-dependent changes in human auditory brainstem evoked responses and contrary to the traditional views that early sensory processing is largely hard-wired, recent studies have revealed that the auditory brainstem is a site where robust synaptic and intrinsic plasticity take place.”
claim-typeexistence— “However, recent groundbreaking results from animal models and human studies have revealed remarkable evidence for cellular and behavioral mechanisms for learning and memory in the auditory brainstem.”
method — evidence— “Contrary to traditional views that early stages of sensory processing are not plastic, new studies discussed in this article have established that the auditory brainstem is dynamic.”
object of study — evidence— “Mechanisms of plasticity have traditionally been ascribed to higher-order sensory processing areas such as the cortex, whereas early sensory processing centers have been considered largely hard-wired. In agreement with this view, the auditory brainstem has been viewed as a nonplastic site, important for preserving temporal information and…
research question — evidence— “A key question is whether the auditory brainstem in mammals expresses the mechanisms that allow activity-dependent modulation of neural circuits and that could support the learning phenomena observed in human studies.”
contribution — evidence— “However, recent groundbreaking results from animal models and human studies have revealed remarkable evidence for cellular and behavioral mechanisms for learning and memory in the auditory brainstem.”
transferfrom visual perception / visual cortical processing: The Reverse Hierarchy Theory, first formulated to describe top-down influence of higher visual cortical areas on lower ones, is taken over to explain top-down modulation of auditory processing and extended below cortex to the brainstem.— “Because the top-down mechanism was originally proposed for the impact of higher-order visual cortical areas to lower-order cortical areas, the focus has been primarily on the intracortical feedback pathway.”transfers[0]
transferfrom electrosensory neurobiology of mormyrid electric fish: The adaptive-sensory-processor / 'negative image' account of anti-Hebbian STDP in the cerebellum-like electrosensory lobe is imported as a candidate functional model for the mammalian dorsal cochlear nucleus.— “The auditory system faces a similar task in that it must differentiate spectral changes in a sound introduced by the animal’s own movements from spectral changes introduced by the movement of an external sound source relative to the animal.”transfers[1]
transferfrom electrosensory neuroscience in mormyrid fish: anti-Hebbian STDP building a negative image that cancels the sensory consequences of the animal's own movements, imported as the candidate function of the dorsal cochlear nucleus— “In this way, anti-Hebbian STDP adjusts parallel fiber synaptic weights in order to sculpt a “negative image” of the neural response caused by the fish’s own movements.”transfers[2]
transferfrom visual perception theory: the Reverse Hierarchy Theory, built for higher-to-lower visual cortical areas and extended here to corticofugal control of the brainstem— “The RHT postulates that the performance of a perceptual task is first based on the highest available level of sensory representation. If the task cannot be accomplished at that level (because of poor sensory resolution), it proceeds down the representational hierarchy to obtain more detailed, lower-level cues that participate in generating…transfers[3]
transferfrom cerebellar physiology: the parallel-fiber and climbing-fiber arrangement, used both as the structural analogy for the DCN and as the model for how auditory nerve activity might induce plasticity— “Cerebellum-like structures act as adaptive sensory processors in which the signals conveyed by parallel fibers in the molecular layer predict the patterns of sensory input to the deep layers through a process of associative anti-Hebbian synaptic plasticity”transfers[4]
mechanismSynapse-specific plasticity simultaneously disinhibits fusiform cells and strengthens their excitatory input, driving the fusiform hyperactivity that underlies tinnitus— “Synapse-specific synaptic plasticity, by decreasing the activity of inhibitory interneurons (disinhibition) and simultaneously increasing excitatory input to fusiform cells, can lead to hyperactivity in fusiform cells, similar to the kind observed in animals with behavioral evidence of tinnitus.”mechanisms[0]
mechanismAnti-Hebbian STDP reweights parallel-fiber synapses so that inputs predicting incoming sensory activity are weakened, building a 'negative image' that cancels the sensory consequences of the animal's own movements— “In this way, anti-Hebbian STDP adjusts parallel fiber synaptic weights in order to sculpt a “negative image” of the neural response caused by the fish’s own movements.”mechanisms[1]
mechanismNitric oxide diffusing out of MNTB principal neurons suppresses postsynaptic Kv3 channels in neighbouring cells, providing intercellular gain control during loud sound— “Diffusion of NO from MNTB principal neurons provides modulatory control of excitability via direct suppression of postsynaptic Kv3 channels”mechanisms[2]
mechanismCorticofugal (efferent) feedback from higher-order processing levels descends onto brainstem nuclei and is the route by which language and musical experience alter subcortical timingmechanisms[3]
mechanismthe field inferred incapacity from function - a structure optimised for fast reliable signalling was assumed to be ill-suited to plasticity, and the test was not runmechanisms[4]
mechanismand effort was directed to the cortex instead, which is where the plasticity literature accumulated
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mechanisms[5]
mechanismthe reversal is built from two independent lines that meet in the middle - slice physiology in animals and non-invasive evoked potentials in humans
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mechanisms[6]
mechanismadding an in-vivo-like feature to the standard slice preparation reversed a standing conclusion about the same nucleus
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mechanisms[7]
mechanismand the authors generalise the warning rather than confining it to that result
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mechanisms[8]
mechanismplasticity is shown to be feature-specific rather than a gain change, which is what makes it evidence of learning rather than of arousal
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mechanisms[9]
mechanismthe functional interpretation of the dorsal cochlear nucleus is imported wholesale from the electrosensory lobe of a fish, where anti-Hebbian plasticity cancels self-generated input
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mechanisms[10]
mechanismthe argument that the same job exists in audition is made by matching the problem, not the anatomy - both systems must separate external signals from self-generated ones
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mechanisms[11]
mechanismhuman timescales are stacked deliberately: lifelong language and musical experience, then training over weeks, then attention within a session
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mechanisms[12]
mechanismthe same plasticity mechanisms are used to explain a pathology, which converts the review's claim into something testable in tinnitus
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mechanisms[13]
mechanisma theory built for visual cortex is extended below the cortex, and the extension is flagged as the authors' view rather than an established result
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mechanisms[14]
extends Reverse Hierarchy Theory (Ahissar and Hochstein, 2004)
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claim_relations[0]
contradicts the traditional view that early sensory processing stages are hard-wired and non-plastic
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claim_relations[1]
critiques the inference from specialisation for precise timing to incapacity for plasticity
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claim_relations[2]
contradicts the treatment of the MNTB as a simple and faithful relay nucleus
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claim_relations[3]
builds-on Krishnan and colleagues, who first showed that language experience alters brainstem pitch encoding
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claim_relations[4]
extends the Reverse Hierarchy Theory, from intracortical feedback to subcortical processing
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claim_relations[5]
supports the account of tinnitus as centrally maintained rather than purely cochlear
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claim_relations[6]
senseSTDP - Hebbian at fusiform cells and anti-Hebbian at cartwheel cells; ONE induction protocol producing opposite signs, decided by cell type
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senses[0]
sensethe auditory brainstem - as a hard-wired relay optimised for timing versus as a plastic, experience-modified structure; the paper is the transition between the two readings
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senses[1]
senseplasticity - synaptic (changed connection strength) versus intrinsic (changed excitability through ion channels); the review insists a circuit needs one or the other
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senses[2]
senseexperience effects - as a generalised gain change versus as feature-specific alteration; only the second counts as learning
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senses[3]
sensethe MNTB - as a simple faithful relay versus as a nucleus that fails under realistic activity; the reading depends on what the slice preparation includes
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senses[4]
sensebrainstem plasticity - as adaptive learning versus as the cause of a disease; the same mechanism read with opposite valence in tinnitus
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senses[5]
edgeHebbian —contrasted-with→ anti-Hebbian
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concept_edges[0]
edgefusiform —contrasted-with→ cartwheel cells
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concept_edges[1]
retractedRETRACTED (WRONG TYPE: a KIND, not a PART) · intrinsic plasticity —is-a→ plasticity — WRONG TYPE: a KIND, not a PART. Intrinsic plasticity is a sort of plasticity, not a component of it.
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concept_edges[2]
weightRETRACTED (WRONG TYPE: a KIND, not a PART) · intrinsic plasticity —is-a→ plasticity — 0.95
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concept_edges[2]
auditfrequency following response —part-of→ auditory brainstem response — Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span writes 'ABR'; endpoint abbreviated.
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concept_edges[3]
auditplasticity —causes→ tinnitus — Audit 2026-09-28: DOUBTFUL - read against its span and kept, but plasticity-driven disinhibition is linked to tinnitus; causes is loose.
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concept_edges[4]
weightplasticity —causes→ tinnitus — 0.75
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concept_edges[4]
weightdorsal cochlear nucleus —part-of→ auditory brainstem — 0.95
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concept_edges[7]
for which uselimitation — every plasticity claim in the review: MOST STUDIES OF SYNAPTIC PLASTICITY IN THE AUDITORY BRAINSTEM HAVE BEEN PERFORMED IN BRAIN SLICES
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limitations[0]
for which uselimitation — the tinnitus account specifically: it is obvious that ELECTRICAL STIMULATION OF PARALLEL FIBERS CAN INDUCE SYNAPTIC PLASTICITY, but how naturally occurring noise exposure would do so is not established
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limitations[1]
for which uselimitation — what the brainstem literature covers: MUCH LESS IS KNOWN ABOUT HOW THESE PATHWAYS ADAPT TO ONGOING SENSORY ACTIVITY AND HOW THEY CONTRIBUTE TO THE PERCEPTION AND INTERPRETATION OF ENVIRONMENTAL SOUNDS, INCLUDING SPEECH
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limitations[2]
for which uselimitation — the plasticity evidence base as a whole: MOST STUDIES OF SYNAPTIC PLASTICITY IN THE AUDITORY BRAINSTEM HAVE BEEN PERFORMED IN BRAIN SLICES. THIS EXPERIMENTAL APPROACH HAS SUBSTANTIAL DIFFERENCES FROM STUDYING INTACT BRAINS IN VIVO
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limitations[3]
duplicate oflimitation — limitations[1]
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limitations[4]
for which uselimitation — the same scope as limitations[1] - how naturally occurring noise exposure would induce the plasticity proposed to underlie tinnitus is not established
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limitations[4]
for which uselimitation — any mechanistic claim about the disorder: DESPITE THE WIDE PREVALENCE OF TINNITUS, THE PATHOPHYSIOLOGY OF THE DISORDER IS POORLY UNDERSTOOD
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limitations[5]
for which uselimitation — the transfer of the cancellation function from the fish circuit: A KEY QUESTION IS WHETHER ANTI-HEBBIAN PLASTICITY OBSERVED IN THE DCN CAN SERVE A SIMILAR FUNCTION
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limitations[6]
for which uselimitation — the locus of control for brainstem plasticity: whether changes are INITIATED/MODULATED IN A TOP-DOWN FASHION ... OR THROUGH LOCAL MECHANISMS OF ADAPTATION is unresolved
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limitations[7]
duplicate oflimitation — limitations[2]
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limitations[8]
for which uselimitation — the same scope as limitations[2] - transmission of timing is understood far better than adaptation or perception
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limitations[8]
replicationuntested
limitationThe synaptic-plasticity evidence base comes overwhelmingly from brain slices, which differ substantially from the intact brain.
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limitations[0]
limitationHow naturally occurring noise exposure would induce the plasticity proposed to underlie tinnitus is not established.
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limitations[1]
limitationHow brainstem pathways adapt to ongoing sensory activity and contribute to perception of environmental sound remains largely unknown.
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limitations[2]
limitationmost of the plasticity evidence comes from slices, which differ from the intact brain in ways that have already changed one conclusion
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limitations[3]
limitationhow noise exposure would induce the plasticity proposed to cause tinnitus is not established
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limitations[4]
limitationthe pathophysiology of tinnitus remains poorly understood despite its prevalence
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limitations[5]
limitationwhether the fish-derived cancellation function applies to the dorsal cochlear nucleus is posed as an open question, not answered
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limitations[6]
limitationwhether brainstem plasticity is driven top-down, locally, or by both is unresolved
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limitations[7]
limitationhow these pathways adapt and contribute to perception is much less understood than how they transmit timing
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limitations[8]
Content tags
content-observations: finding · quantity · variable · definition · key-term — grounded in the full text
findingContrary to the traditional view that early sensory stages are not plastic, the auditory brainstem is dynamic.
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content_tags.findings[0]
findingIn the dorsal cochlear nucleus one protocol produces LTP in fusiform cells and LTD in cartwheel cells.
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content_tags.findings[1]
findingLanguage experience reshapes brainstem coding: speakers of tonal languages show enhanced neural representation of pitch.
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content_tags.findings[2]
findingExperience-driven changes in the brainstem are selective to particular stimulus features rather than an across-the-board amplification of all responses.
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content_tags.findings[3]
findingAcoustic environment tunes intrinsic excitability: in quiet conditions PKC phosphorylation of Kv3.1b potassium channels lowers the potassium current so that neurons fire only at low frequencies.
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content_tags.findings[4]
findingThe medial nucleus of the trapezoid body is not a faithful relay: under in-vivo-like spontaneous activity it fails to entrain reliably to prolonged high-frequency stimuli because of short-term plasticity, even though it still encodes stimulus onset precisely.
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content_tags.findings[5]
findingThe authors argue that the Reverse Hierarchy Theory, formulated for cortex, extends to subcortical processing and may itself initiate or modulate brainstem plasticity.
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content_tags.findings[6]
findingone induction protocol produces LTP in fusiform cells and LTD in cartwheel cells
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content_tags.findings[7]
findingspeakers of tonal languages have enhanced neural representation of pitch in the brainstem
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content_tags.findings[8]
findingmusical experience produces more robust brainstem encoding of speech, linguistic pitch patterns and vocal emotion
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content_tags.findings[9]
findingbrainstem encoding is disrupted in subsets of poor readers and children with autism
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content_tags.findings[10]
findingbrainstem responses are affected by attention and are larger to a speech syllable than to its time-reversed version
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content_tags.findings[11]
findingexperience does not produce a generalised gain change but alters specific stimulus features
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content_tags.findings[12]
findingbrainstem processing can also be changed by auditory training over weeks, not only by lifelong experience
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content_tags.findings[13]
findingadding in-vivo-like spontaneous activity to MNTB slices revealed synaptic failures at high frequency that earlier studies had not seen
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content_tags.findings[14]
findingso the MNTB is not a simple faithful relay and may not entrain reliably to sustained high-frequency input
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content_tags.findings[15]
findingphosphorylation state of Kv3.1b channels sets whether neurons fire at low or high frequency, tracking the acoustic environment
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content_tags.findings[16]
findingactivity in one MNTB neuron can modulate the excitability of its neighbours, a candidate gain reduction in loud noise
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content_tags.findings[17]
findingretrograde GABA signalling in the lateral superior olive adjusts the excitation-inhibition balance underlying sound localisation
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content_tags.findings[18]
findingsynapse-specific plasticity that disinhibits and excites fusiform cells can produce hyperactivity like that seen in animals with behavioural signs of tinnitus
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content_tags.findings[19]
findingcortical activation shapes the tuning of cochlear nucleus neurons, giving a route for top-down control
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content_tags.findings[20]
quantity<4000 Hz — Upper frequency limit of the 'low-frequency' sounds that the binaural timing circuitry of the mammalian brainstem is specialised to localise
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content_tags.quantities[0]
quantity4–12 µm — Diameter of the myelinated globular-bushy-cell axons giving rise to the calyx of Held, large enough to give fast conduction velocity
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content_tags.quantities[1]
quantity200 µs — Delay with which inhibitory input reaches the cat lateral superior olive after the excitatory input
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content_tags.quantities[2]
quantity40 ms time bins, 1 ms interval — Window length and step of the running short-term Fourier analysis used to extract pitch contours from the brainstem response
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content_tags.quantities[3]
quantity0.5 ms — Scale of the x-axis tick marks in Figure 1, indicating that the experience-related timing disruptions and enhancements are of the order of tenths of a millisecond
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content_tags.quantities[4]
quantity<4000 Hz — the low-frequency range localised by interaural timing in mammals
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content_tags.quantities[5]
quantitymicrosecond range — the interaural phase differences the brainstem resolves
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content_tags.quantities[6]
quantitylast 10 years — the period over which brainstem timing mechanisms were worked out
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content_tags.quantities[7]
variablerelative timing of presynaptic and postsynaptic action potentials
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content_tags.variables[0]
variablesound intensity
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content_tags.variables[1]
variablepitch tracking
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content_tags.variables[2]
definitionintrinsic plasticity
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content_tags.definitions[0]
definitionspike-timing-dependent plasticity (STDP)
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content_tags.definitions[1]
definitionauditory brainstem response (ABR)
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content_tags.definitions[2]
definitionfrequency following response (FFR)
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content_tags.definitions[3]
definitiontinnitus
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content_tags.definitions[4]
definitionpitch tracking
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content_tags.definitions[5]
definitionReverse Hierarchy Theory (RHT)
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content_tags.definitions[6]
definitionauditory brainstem response
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content_tags.definitions[7]
definitionfrequency following response
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content_tags.definitions[8]
definitionspike-timing-dependent plasticity
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content_tags.definitions[9]
definitionintrinsic plasticity
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content_tags.definitions[10]
definitionTinnitus
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content_tags.definitions[11]
definitionReverse Hierarchy Theory
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content_tags.definitions[12]
key-termsauditory brainstem, plasticity, intrinsic plasticity, spike-timing-dependent plasticity, Hebbian, anti-Hebbian, long-term potentiation, long-term depression, dorsal cochlear nucleus, fusiform, cartwheel cells, auditory brainstem response, frequency following response, phase locking, pitch tracking, interaural time differences, Reverse Hierarchy Theory, corticofugal, tinnitus, Kv3.1b, negative image, musicians, calyx of Held, superior olivary complex, cochlear nucleus, nitric oxide
Concepts
terms this paper carries, each with the sentence it was cut from — the layer that joins one paper to another. Terms with no quote yet are on CONCEPTS.html.
conceptauditory brainstem response — not defined in this paper's own words; ABR, the non-invasive far-field measure of stimulus-locked brainstem activity
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concepts[12]
Statistics — cross-field join keys
field-invariant statistical terms, used in their statistical sense (gated on a number / symbol / test). A p-value or a standard deviation means the SAME thing in physics, biology, psychology and sociology — so these are the strongest cross-field join keys. Grounded verbatim.
standard error of the mean SEM as written: ±SEM
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content_tags.statistics[0]
fast Fourier transform
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content_tags.statistics[1]
phase locking
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content_tags.statistics[2]
Second readings
a facet read a second time, independently, from its own sentence — and whether the two readings agree
claim typecritique — a second reading DIFFERING from the recorded value; recorded: existence
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alternatives.claim_type
methodnarrative review pairing rodent brain-slice recordings of synaptic and intrinsic plasticity with non-invasive human auditory brainstem responses — a second reading DIFFERING from the recorded value; recorded: review
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alternatives.method
phenomenonexperience-dependent plasticity in subcortical auditory processing — a second reading DIFFERING from the recorded value; recorded: auditory brainstem plasticity
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alternatives.phenomenon

When we have changed our mind. Some entries in the table begin with a word in capitals and the reason for it. EVIDENCE CORRECTED — the finding still stands, but we had quoted the wrong sentence from the paper, and the quotation has been replaced with the right one. RETRACTED — the entry itself was wrong; it stays on the page, marked, with the reason, rather than being deleted. WITHDRAWN AND REPLACED — the entry was wrong, and a corrected version of it appears in the entries below. Each mark carries its own reason, in brackets, because the reasons differ from one entry to the next. An entry we have WITHDRAWN is removed from this page and kept in the record, with its reason. A line reading Audit and a date is a later re-reading of the entry against its whole sentence: DOUBTFUL means it was kept, and the reason says what is loose about it. Quotation marks inside the tagger's sentence. Where a tag is the tagger's own sentence, a phrase in quotation marks inside it is borrowed from the paper — the tagger's wording around it is not. The paper's own sentence is the evidence quote for that row; on this page it is withheld with the article, and the article is at its publisher. Nothing inside quotation marks anywhere on this page is ours: if it is quoted, it is the paper's. Whose words a concept carries. A concept entry records a term the paper itself uses, so the term, the sense given for it, and its evidence are the paper's own words, quoted where the paper fixes them. This is the opposite of a sense entry in the tag table, which is the tagger's sentence about how the paper uses a term. Where a concept entry could not be grounded in the paper's words, the entry says so on its own row.

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