Auditory midbrain coding of statistical learning that results from discontinuous sensory stimulation

Cruces-Solis, Hugo; Jing, Zhizi; Babaev, Olga; Rubin, Jonathan E.; Gür, Burak; Krueger‐Burg, Dilja; Strenzke, Nicola; Hoz, Livia de

doi:10.1371/journal.pbio.2005114

Cited by 29 publications

(57 citation statements)

References 94 publications

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“…Initially, we trained mice in a pure-tone frequency discrimination task that resembled a go/no-go discrimination paradigm. Importantly, most visits, over two thirds, are spaced by intervals of more than 1 minute (S1D Fig; [25]) and tone frequency judgement must, therefore, rely on memory. In those visits in which the ‘safe sound’ was presented (safe visits), mice had access to water through a nose-poke on either side of corner (S1B-top Fig), whereas when the ‘conditioning sound’ was played (conditioned visits), nose-poking on either side was followed by an aversive air puff and no access to water (S1B-bottom Fig).…”

Section: Resultsmentioning

confidence: 99%

Wide sensory filters underlie performance in memory-based discrimination and generalization

2019

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The way animals respond to a stimulus depends largely on an internal comparison between the current sensation and the memory of previous stimuli and outcomes. We know little about the accuracy with which the physical properties of the stimuli influence this type of memory-based discriminative decisions. Research has focused largely on discriminations between stimuli presented in quick succession, where animals can make relative inferences (same or different; higher or lower) from trial to trial. In the current study we used a memory-based task to explore how the stimulus’ physical properties, in this case tone frequency, affect auditory discrimination and generalization in mice. Mice performed ad libitum while living in groups in their home quarters. We found that the frequency distance between safe and conditioned sounds had a constraining effect on discrimination. As the safe-to-conditioned distance decreased across groups, performance deteriorated rapidly, even for frequency differences significantly larger than reported discrimination thresholds. Generalization width was influenced both by the physical distance and the previous experience of the mice, and was not accompanied by a decrease in sensory acuity. In conclusion, memory-based discriminations along a single stimulus dimension are inherently hard, reflecting a high overlap between the memory traces of the relevant stimuli. Memory-based discriminations rely therefore on wide sensory filters.

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Section: Resultsmentioning

confidence: 99%

Wide sensory filters underlie performance in memory-based discrimination and generalization

2019

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“…The AudioBox system was used to test behavioral gap-detection. The AudioBox (New Behavior , TSE systems) is an automated system for behavioral acoustic conditioning 69–72 . This system is designed to minimize the interference from the experimenter and provides a spatially and socially enriched environment in which female mice live in group (up to 10 mice) for several days.…”

Section: Methodsmentioning

confidence: 99%

“…A speaker was over the corner (22TAF/G, Seas Prestige). Animals carried a transponder (implanted under anesthesia, see 72 ) that was detected by an antenna at the entrance of the corner. Time spent in the corner, number of nose-pokes and sound played were detected through sensors in the corner.…”

Section: Methodsmentioning

confidence: 99%

A role of oligodendrocytes in information processing independent of conduction velocity

Moore

Meschkat

Ruhwedel

et al. 2019

Preprint

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41Myelinating oligodendrocytes enable fast impulse propagation along axons as revealed 42 through studies of homogeneously myelinated white matter tracts. However, gray matter 43 myelination patterns are different, with sparsely myelinated sections leaving large 44 portions of the axons naked. The consequences of this patchy myelination for 45 oligodendrocyte function are not understood but suggest other roles in information 46 processing beyond the regulation of axonal conduction velocity. Here, we analyzed the 47 contribution of myelin to auditory information processing using paradigms that are good 48 predictors of speech understanding in humans. We compared mice with different degrees 49 of dysmyelination using acute cortical multiunit recordings in combination with behavioral 50 readouts. We identified complex alterations of neuronal responses that reflect fatigue and 51 temporal acuity deficits. Partially discriminable but overall similar deficits were observed 52 in mice with oligodendrocytes that can myelinate but cannot fully support axons 53 metabolically. Thus, myelination contributes to sustained stimulus perception in 54 temporally complex paradigms, revealing a role of oligodendrocytes in the CNS beyond 55 the increase of axonal conduction velocity. 56 65 66Importantly, at the network level, the contribution of CNS myelination to information 67 processing remains poorly understood, in part because suitable phenotyping instruments 68 have been lacking. Yet, there is an increasing awareness that myelination is required for 69 higher-order brain functions. Subtle defects of the white matter have been associated with 70 various psychiatric diseases 6 . Moreover, in the aging brain, the physiological decline of 71 function is associated with subtle but widespread structural deterioration of myelin 7,8 . 72Functional studies of myelin have largely been restricted to motor behavior, which is 73 under control of myelinated axons in white matter tracts, and to the fast impulse 74 propagation and millisecond precision required for sound location in a highly specialized 75 circuit of the brain stem 9 . However, myelin is also present within the cortical grey matter, 76 where it is heterogeneous and patchy along projection neurons 10,11 . Moreover, a large 77 fraction of the parvalbumin-positive interneuron axons are myelinated 12-14 , even though 78 their typical short distance to their target cells has been estimated to cause insignificant 79 conduction delay times 13 . Oligodendrocyte lineage cells can myelinate axons in an 80 activity dependent manner and influence their conduction velocity properties [15][16][17][18][19] . Mature 81 oligodendrocytes respond to glutamatergic signals with enhanced glycolytic support of 82 the axonal energy metabolism 4,5 . These data are compatible with the idea that myelin 83 function in the CNS that go beyond regulating conduction velocity. 85Indeed, there is still a major conceptual gap between the role of myelin in saltatory 86 impulse propagation and its function ...

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“…This suggests that the differences in response to conspecific and heterospecific songs recorded in MLd are not simply a result of repeated exposure to a particular auditory stimulus. Repeated exposure has been shown to change neural responses in the auditory cortex of rats (Bao et al, 2013), ferrets (Schnupp et al, 2006), and gerbils (Caras & Sanes, 2017), and in the auditory midbrain of mice (Cruces-Solís et al, 2018) and frogs (Gall & Wilczynski, 2014). Instead, the persistence of the differences observed in the MLd of both groups of birds, suggest that these changes may be influenced by the critical period of learning associated with song learning.…”

Section: Resultsmentioning

confidence: 99%

Auditory processing in the zebra finch midbrain: single unit responses and effect of rearing experience

Logerot

Smith

Wild

et al. 2020

PeerJ

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In birds the auditory system plays a key role in providing the sensory input used to discriminate between conspecific and heterospecific vocal signals. In those species that are known to learn their vocalizations, for example, songbirds, it is generally considered that this ability arises and is manifest in the forebrain, although there is no a priori reason why brainstem components of the auditory system could not also play an important part. To test this assumption, we used groups of normal reared and cross-fostered zebra finches that had previously been shown in behavioural experiments to reduce their preference for conspecific songs subsequent to cross fostering experience with Bengalese finches, a related species with a distinctly different song. The question we asked, therefore, is whether this experiential change also changes the bias in favour of conspecific song displayed by auditory midbrain units of normally raised zebra finches. By recording the responses of single units in MLd to a variety of zebra finch and Bengalese finch songs in both normally reared and cross-fostered zebra finches, we provide a positive answer to this question. That is, the difference in response to conspecific and heterospecific songs seen in normal reared zebra finches is reduced following cross-fostering. In birds the virtual absence of mammalian-like cortical projections upon auditory brainstem nuclei argues against the interpretation that MLd units change, as observed in the present experiments, as a result of top-down influences on sensory processing. Instead, it appears that MLd units can be influenced significantly by sensory inputs arising directly from a change in auditory experience during development.

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Auditory midbrain coding of statistical learning that results from discontinuous sensory stimulation

Cited by 29 publications

References 94 publications

Wide sensory filters underlie performance in memory-based discrimination and generalization

Wide sensory filters underlie performance in memory-based discrimination and generalization

A role of oligodendrocytes in information processing independent of conduction velocity

Auditory processing in the zebra finch midbrain: single unit responses and effect of rearing experience

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