Sensory overamplification in layer 5 auditory corticofugal projection neurons following cochlear nerve synaptic damage

Asokan, Meenakshi M.; Williamson, R. S.; Hancock, Kenneth E.; Polley, Daniel B.

doi:10.1038/s41467-018-04852-y

Cited by 91 publications

(84 citation statements)

References 73 publications

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“…In mice exposed to the same traumatic noise used here, both SR and tone rate-level slopes were transiently increased in auditory cortical neurons 3-4 days post exposure, recovering to baseline by 1 wk (Resnik and Polley, 2017). Again using the same noise exposure, calcium imaging of cortico-collicular neurons revealed increased rate-level slopes 2 days post exposure that remained elevated to at least 2 wks (Asokan et al, 2018). Here, we didn't track neuronal responsiveness at post-exposure times < 1 wk, when larger effects might have been seen.…”

Section: Effects Of Noise Exposure On Sound-evoked Responsesmentioning

confidence: 54%

“…Most prior work on noise-induced central hyperactivity did not quantify the condition of hair cells and/or cochlear nerve fibers, nor the possible correlations between peripheral histopathology and central pathophysiology (but see Hesse et al, 2016;Asokan et al, 2018). While identically exposed animals develop behavioral evidence of tinnitus at rates ranging from 30 to 70% (Engineer et al, 2011;Dehmel et al, 2012b;Li et al, 2013;Rüttiger et al, 2013), these studies did not ask whether variability was related to differences in peripheral insult.…”

Section: Introductionmentioning

confidence: 99%

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Effects of cochlear synaptopathy on spontaneous and sound-evoked activity in the mouse inferior colliculus

Liberman

2018

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Tinnitus and hyperacusis are life-disrupting perceptual abnormalities that are often preceded by acoustic overexposure. Animal models of overexposure have suggested a link between these phenomena and neural hyperactivity, i.e. elevated spontaneous rates (SRs) and soundevoked responses. Prior work has focused on changes in central auditory responses, with less attention paid to the exact nature of the associated peripheral damage. The demonstration that acoustic overexposure can cause cochlear nerve damage without permanent threshold elevation suggests this type of peripheral damage may be a key elicitor of tinnitus and hyperacusis in humans with normal audiograms. We addressed this idea by recording responses in the mouse inferior colliculus (IC) following a bilateral, neuropathic noise exposure. Two wks post-exposure, mean SRs were unchanged in mice recorded while awake, or under anesthesia. SRs were also unaffected by more intense, or unilateral exposures. These results suggest that neither neuropathy nor hair cell loss are sufficient to raise SRs in the IC, at least in mice. However, it's not clear whether our mice had tinnitus. Tone-evoked rate-level functions at the CF were steeper following exposure, specifically in the region of maximal neuropathy. Furthermore, suppression driven by off-CF tones and by ipsilateral noise were also reduced. Both changes were especially pronounced in neurons of awake mice. These findings align with prior reports of elevated acoustic startle in neuropathic mice, and indicate that neuropathy may initiate a compensatory response in the central auditory system leading to the genesis of hyperacusis.

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Section: Effects Of Noise Exposure On Sound-evoked Responsesmentioning

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Effects of cochlear synaptopathy on spontaneous and sound-evoked activity in the mouse inferior colliculus

Liberman

2018

Preprint

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“…Thus, coordination appears to span the highest to lowest levels of the auditory system, which is consistent with previous corticofugal interpretations of long-lasting experience-dependent plasticity in the human ABR 42 and the brainstem's frequency-following response (FFR) 43 . Indeed, the interaction between cortical and subcortical sound-evoked responses is not new 44 , which includes evidence of cortical re-organization of descending inputs after early auditory system damage 45 . The present findings relate these interactions to adult learning-dependent effects.…”

Section: Discussionmentioning

confidence: 99%

Precise Memory is Predicted by Learning-Induced Sensory System Neurophysiological Plasticity

Rotondo

Bieszczad

2019

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Despite identical learning experiences, individuals differ in the memory formed of those experiences. Memory formed with sensory specificity determines its utility for selectively cueing subsequent behavior, even in novel situations. If an individual forms generalized memory, then there is potential for novel sensory cues to interfere with accurate behavioral performance. Here, a rodent model of auditory learning capitalized on individual differences in learning-induced auditory neuroplasticity to identify and characterize neural substrates for sound-specific (vs. general) memory of the training signal's acoustic frequency. Animals with naturally or pharmacologically induced signal-"specific" memory revealed behaviorally, exhibited longlasting signal-specific neurophysiological plasticity in auditory cortical and subcortical evoked responses, while learning-induced changes were not detected in animals with "general" memories. Individual differences validated this brain-behavior relationship, such that the degree of change in neurophysiological responses could be used to determine the precision of memory formation. Main Text:Individual differences are often intentionally minimized by experimental designs in behavioral neuroscience. Consequently, traditional approaches implicitly treat differences between subjects as "noise" to be overcome by large enough sample sizes to accurately describe and compare the underlying distributions of each group. This philosophical choice stymies an opportunity to use variability as a key to understand brain-behavior relationships. Even when group analyses reveal significant effects, they may not identify the full extent of brain-behavior relationships. Variability in learning, memory, and behavior derives from multiple factors 1-8 each with their own neural generators that have distinct effects on function 9-11 . Therefore, a powerful use of within-group variability is to explain magnitude-of-effect in individual behavioral performance by differences in learning-induced neural function. Indeed, a major goal in behavioral neuroscience is to understand brain-behavior relationships enough to gain the ability to manipulate function and drive behavior in a desired direction by promoting neuroplasticity [12][13][14] . However, to harness plasticity mechanisms in a useful way after the form of experience-induced plasticity between groups is identified, its function and magnitude of effect must be determined at the level of the individual.Previous work has identified distinct functions for different forms of auditory system plasticity related to the behavioral relevance of acoustic frequency 6,15-18 including at different time scales [19][20][21] . For example, in the auditory cortex, rapid changes in neural tuning properties correlate with selective attention to sound frequency during active tasks 21,22 , while long-term changes in tuning bandwidth may be related to frequency-specific memory over time 23,24 . Subcortical neurons in the lemniscal auditory nuclei also exhibit changes in tun...

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“…we used an intersectional virus strategy that exploited their divergent axons fields that also innervate the tectum (Asokan et al 2018). We first injected canine adenovirus 2 (CAV2-Cre) 92 into the inferior colliculus, which selectively infects local axon terminals to express retrogradely 5 in upstream projection neurons (N=6 mice, Figure 1A: left) (Soudais et al 2001;Schneider et al 94 2014; Liu et al 2016).…”

Section: Two Types Of Corticothalamic Projection Neuronsmentioning

confidence: 99%

Parallel systems for sound processing and functional connectivity among layer 5 and 6 auditory corticothalamic neurons

Williamson

2018

Preprint

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Cortical layers (L) 5 and 6 are populated by a spatially intermingled menagerie of 28 neurons with distinct inputs and downstream targets. Here, we made optogenetically guided recordings from L5 and L6 corticothalamic (CT) neurons in the mouse auditory cortex to discern 30 underlying patterns of functional connectivity and sensory processing in the largest sub-cerebral projection system. Whereas L5 CT neurons showed broad stimulus selectivity with sluggish 32 response latencies and extended temporal non-linearities, L6 CTs exhibited sparse sound feature selectivity and rapid temporal processing. L5 CT spikes lagged behind neighboring units and 34 imposed weak feedforward excitation within the local column. By contrast, L6 CT spikes drove robust and sustained activity in neighboring units. Our findings underscore a duality among CT 36 projection neurons, where L5 CT units are canonical broadcast neurons that integrate sensory inputs for transmission to distributed downstream targets, while L6 CT neurons are positioned to 38 regulate thalamocortical response gain and selectivity.40

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Sensory overamplification in layer 5 auditory corticofugal projection neurons following cochlear nerve synaptic damage

Cited by 91 publications

References 73 publications

Effects of cochlear synaptopathy on spontaneous and sound-evoked activity in the mouse inferior colliculus

Effects of cochlear synaptopathy on spontaneous and sound-evoked activity in the mouse inferior colliculus

Precise Memory is Predicted by Learning-Induced Sensory System Neurophysiological Plasticity

Parallel systems for sound processing and functional connectivity among layer 5 and 6 auditory corticothalamic neurons

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