Development of myelination and cholinergic innervation in the central auditory system of a prosimian primate (<i>Otolemur garnetti</i>)

Miller, Daniel J.; Lackey, Elizabeth P.; Hackett, Troy A.; Kaas, Jon H.

doi:10.1002/cne.23379

Cited by 15 publications

(19 citation statements)

References 78 publications

(116 reference statements)

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“…In Wt mice, all auditory projections, including the auditory nerve, are well myelinated 39 , 40 . Before studying the effect of dysmyelination on information processing, we determined latencies and amplitudes of sound-evoked responses at different auditory stations using auditory brainstem responses (ABR), recorded in vivo through electrodes located over the scalp (Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

A role of oligodendrocytes in information processing

et al. 2020

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Myelinating oligodendrocytes enable fast propagation of action potentials along the ensheathed axons. In addition, oligodendrocytes play diverse non-canonical roles including axonal metabolic support and activity-dependent myelination. An open question remains whether myelination also contributes to information processing in addition to speeding up conduction velocity. Here, we analyze the role of myelin in auditory information processing using paradigms that are also good predictors of speech understanding in humans. We compare mice with different degrees of dysmyelination using acute multiunit recordings in the auditory cortex, in combination with behavioral readouts. We find complex alterations of neuronal responses that reflect fatigue and temporal acuity deficits. We observe partially discriminable but similar deficits in well myelinated mice in which glial cells cannot fully support axons metabolically. We suggest a model in which myelination contributes to sustained stimulus perception in temporally complex paradigms, with a role of metabolically active oligodendrocytes in cortical information processing.

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Section: Resultsmentioning

confidence: 99%

A role of oligodendrocytes in information processing

et al. 2020

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“…In wild type mice, all auditory projections, including the auditory nerve, are well myelinated 39,40 . Before studying the effect of dysmyelination on information processing, we determined latencies and amplitudes of sound-evoked responses at different auditory stations using auditory brainstem responses (ABR), recorded in vivo through electrodes located on the scalp (Figure 1A i).…”

Section: Resultsmentioning

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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“…In the MGB, latencies of inhibitory postsynaptic responses reduce from P16 to P27 in rats (Venkataraman and Bartlett, ). The reduction of synaptic latencies in turn can arise from faster conduction velocity due to increased myelination (Hildebrand and Waxman, ; Miller et al, ), faster presynaptic APs (Venkataraman and Bartlett, ), or an increase in vesicle exocytosis (Johnson et al, ).…”

Section: Discussionmentioning

confidence: 99%

Postnatal development of auditory central evoked responses and thalamic cellular properties

Venkataraman

Bartlett

2013

Developmental Neurobiology

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During development, the sense of hearing changes rapidly with age, especially around hearing onset. During this period, auditory structures are highly sensitive to alterations of the acoustic environment, such as hearing loss or background noise. This sensitivity includes auditory temporal processing, which is important for processing complex sounds, and for acquiring reading and language skills. Developmental changes can be observed at multiple levels of brain organization-from behavioral responses to cellular responses, and at every auditory nucleus. Neuronal properties and sound processing change dramatically in auditory cortex neurons after hearing onset. However, development of its primary source, the auditory thalamus, or medial geniculate body (MGB), has not been well studied over this critical time window. Furthermore, to understand how temporal processing develops, it is important to determine the relative maturation of temporal processing not only in the MGB, but also in its inputs. Cellular properties of rat MGB neurons were studied using in vitro whole-cell patch-clamp recordings, at ages postnatal day (P) 7-9; P15-17, and P22-32. Auditory evoked potentials were measured in P14-17 and P22-32 rats. MGB action potentials became about five times faster, and the ability to generate spike trains increased with age, particularly at frequencies of 50 Hz and higher. Evoked potential responses, including auditory brainstem responses (ABR), middle latency responses (MLR), and amplitude modulation following responses, showed increased amplitudes with age, and ABRs and MLRs additionally showed decreased latencies with age. Overall, temporal processing at subthalamic nuclei is concurrently maturing with MGB cellular properties.

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Development of myelination and cholinergic innervation in the central auditory system of a prosimian primate (Otolemur garnetti)

Cited by 15 publications

References 78 publications

A role of oligodendrocytes in information processing

A role of oligodendrocytes in information processing

A role of oligodendrocytes in information processing independent of conduction velocity

Postnatal development of auditory central evoked responses and thalamic cellular properties

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