Shorter cortical adaptation in dyslexia is broadly distributed in the superior temporal lobe and includes the primary auditory cortex

Studies of the performance of individuals with dyslexia in perceptual tasks suggest that their implicit inference of sound statistics is impaired. Previously, using two-tone frequency discrimination, we found that the effect of previous trials' frequencies on the judgments of individuals with dyslexia decays faster than the effect on controls' judgments, and that the adaptation (decrease of neural response to repeated stimuli) of their ERP responses to tones is shorter (<xref ref-type="bibr" rid="bib22">Jaffe-Dax et al., 2017</xref>). Here, we show the cortical distribution of these abnormal dynamics of adaptation using fast-acquisition fMRI. We find that faster decay of adaptation in dyslexia is widespread, although the most significant effects are found in the left superior temporal lobe, including the auditory cortex. This broad distribution suggests that the faster decay of implicit memory of individuals with dyslexia is a general characteristic of their cortical dynamics, which also affects sensory cortices.

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Widespread shorter cortical adaptation in dyslexia

10.1101/219923 ◽

2017 ◽

Author(s):

Sagi Jaffe-Dax ◽

Eva Kimel ◽

Merav Ahissar

Keyword(s):

General Characteristic ◽

Frequency Discrimination ◽

Previous Trial ◽

Tone Frequency ◽

Broad Distribution ◽

Cortical Dynamics ◽

Fast Acquisition ◽

Sensory Cortices ◽

Cortical Adaptation ◽

Cortical Distribution

AbstractStudies of dyslexics’ performance on perceptual tasks suggest that their implicit inference of sound statistics is impaired. In a previous paper (Jaffe-Dax, Frenkel, & Ahissar, 2017), using 2-tone frequency discrimination, we found that the effect of previous trial frequencies on dyslexics’ judgments decayed faster than the effect on controls’ judgments, and that the adaptation of their ERP responses to tones recovered faster. Here, we show the cortical distribution of this abnormal dynamics of adaptation using fast acquisition fMRI. We find that dyslexics’ faster decay of adaptation is widespread, though the most significant effects are found in the left superior temporal lobe, including the auditory cortex. This broad distribution suggests that dyslexics’ faster decay of implicit memory is a general characteristic of their cortical dynamics, which also encompasses the sensory cortices.

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Author response: Shorter cortical adaptation in dyslexia is broadly distributed in the superior temporal lobe and includes the primary auditory cortex

10.7554/elife.30018.009 ◽

2018 ◽

Author(s):

Sagi Jaffe-Dax ◽

Eva Kimel ◽

Merav Ahissar

Keyword(s):

Auditory Cortex ◽

Temporal Lobe ◽

Primary Auditory Cortex ◽

Author Response ◽

Cortical Adaptation

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Decision letter: Shorter cortical adaptation in dyslexia is broadly distributed in the superior temporal lobe and includes the primary auditory cortex

10.7554/elife.30018.008 ◽

2018 ◽

Keyword(s):

Auditory Cortex ◽

Temporal Lobe ◽

Primary Auditory Cortex ◽

Cortical Adaptation

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Short-term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

10.1101/2019.12.19.883165 ◽

2019 ◽

Author(s):

Jesyin Lai ◽

Stephen V. David

Keyword(s):

Auditory Cortex ◽

Vagus Nerve ◽

Nerve Stimulation ◽

Neural Activity ◽

Neural Plasticity ◽

Neural Coding ◽

Vagus Nerve Stimulation ◽

Primary Auditory Cortex ◽

Long Term Effects ◽

Tone Frequency

ABSTRACTChronic vagus nerve stimulation (VNS) can facilitate learning of sensory and motor behaviors. VNS is believed to trigger release of neuromodulators, including norepinephrine and acetylcholine, which can mediate cortical plasticity associated with learning. Most previous work has studied effects of VNS over many days, and less is known about how acute VNS influences neural coding and behavior over the shorter term. To explore this question, we measured effects of VNS on learning of an auditory discrimination over 1-2 days. Ferrets implanted with cuff electrodes on the vagus nerve were trained by classical conditioning on a tone frequency-reward association. One tone was associated with reward while another tone, was not. The frequencies and reward associations of the tones were changed every two days, requiring learning of a new relationship. When the tones (both rewarded and non-rewarded) were paired with VNS, rates of learning increased on the first day following a change in reward association. To examine VNS effects on auditory coding, we recorded single- and multi-unit neural activity in primary auditory cortex (A1) of passively listening animals following brief periods of VNS (20 trials/session) paired with tones. Because afferent VNS induces changes in pupil size associated with fluctuations in neuromodulation, we also measured pupil during recordings. After pairing VNS with a neuron’s best-frequency (BF) tone, responses in a subpopulation of neurons were reduced. Pairing with an off-BF tone or performing VNS during the inter-trial interval had no effect on responses. We separated the change in A1 activity into two components, one that could be predicted by fluctuations in pupil and one that persisted after VNS and was not accounted for by pupil. The BF-specific reduction in neural responses remained, even after regressing out changes that could be explained by pupil. In addition, the size of VNS-mediated changes in pupil predicted the magnitude of persistent changes in the neural response. This interaction suggests that changes in neuromodulation associated with arousal gate the long-term effects of VNS on neural activity. Taken together, these results support a role for VNS in auditory learning and help establish VNS as a tool to facilitate neural plasticity.

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Pairing Cholinergic Enhancement with Perceptual Training Promotes Recovery of Age-Related Changes in Rat Primary Auditory Cortex

Neural Plasticity ◽

10.1155/2016/1801979 ◽

2016 ◽

Vol 2016 ◽

pp. 1-18 ◽

Cited By ~ 13

Author(s):

Patrice Voss ◽

Maryse Thomas ◽

You Chien Chou ◽

José Miguel Cisneros-Franco ◽

Lydia Ouellet ◽

...

Keyword(s):

Auditory Cortex ◽

Structural Changes ◽

Primary Auditory Cortex ◽

Auditory Training ◽

Tone Frequency ◽

Perceptual Training ◽

Adult Rats ◽

Functional Changes ◽

Age Related ◽

Old Rats

We used the rat primary auditory cortex (A1) as a model to probe the effects of cholinergic enhancement on perceptual learning and auditory processing mechanisms in both young and old animals. Rats learned to perform a two-tone frequency discrimination task over the course of two weeks, combined with either the administration of a cholinesterase inhibitor or saline. We found that while both age groups learned the task more quickly through cholinergic enhancement, the young did so by improving target detection, whereas the old did so by inhibiting erroneous responses to nontarget stimuli. We also found that cholinergic enhancement led to marked functional and structural changes within A1 in both young and old rats. Importantly, we found that several functional changes observed in the old rats, particularly those relating to the processing and inhibition of nontargets, produced cortical processing features that resembled those of young untrained rats more so than those of older adult rats. Overall, these findings demonstrate that combining auditory training with neuromodulation of the cholinergic system can restore many of the auditory cortical functional deficits observed as a result of normal aging and add to the growing body of evidence demonstrating that many age-related perceptual and neuroplastic changes are reversible.

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Facilitatory and Inhibitory Frequency Tuning of Combination-Sensitive Neurons in the Primary Auditory Cortex of Mustached Bats

Journal of Neurophysiology ◽

10.1152/jn.1999.82.5.2327 ◽

1999 ◽

Vol 82 (5) ◽

pp. 2327-2345 ◽

Cited By ~ 42

Author(s):

Jagmeet S. Kanwal ◽

Douglas C. Fitzpatrick ◽

Nobuo Suga

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Temporal Structure ◽

Primary Auditory Cortex ◽

Frequency Discrimination ◽

Inhibitory Response ◽

Center Frequency ◽

Constant Frequency ◽

Single Tone ◽

Threshold Response

Mustached bats, Pteronotus parnellii parnellii,emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF1-4) component followed by a short, frequency-modulated (FM1-4) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF2 is maintained within a narrowband centered at ∼61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63.0-kHz frequencies in the “Doppler-shifted CF processing” (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of ∼25 kHz (BFlow) and ∼61 kHz (BFhigh). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BFlowcorresponding to a frequency in the lower half of the echolocation pulse FM1 sweep and another of sharp tuning to frequencies centered at BFhigh corresponding to the CF2 in the echo. Facilitative response areas for BFhigh are broadened by ∼0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BFhigh response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BFhigh. About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BFhigh so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BFhigh and sometimes for BFlow. Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.

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Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00682.2014 ◽

2015 ◽

Vol 113 (2) ◽

pp. 475-486

Author(s):

Melanie A. Kok ◽

Daniel Stolzberg ◽

Trecia A. Brown ◽

Stephen G. Lomber

Keyword(s):

Auditory Cortex ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Population Level ◽

Noise Burst ◽

Hierarchical Organization ◽

Neuronal Responses ◽

Tone Frequency ◽

Hierarchical Processing ◽

Auditory Field

Current models of hierarchical processing in auditory cortex have been based principally on anatomical connectivity while functional interactions between individual regions have remained largely unexplored. Previous cortical deactivation studies in the cat have addressed functional reciprocal connectivity between primary auditory cortex (A1) and other hierarchically lower level fields. The present study sought to assess the functional contribution of inputs along multiple stages of the current hierarchical model to a higher order area, the dorsal zone (DZ) of auditory cortex, in the anaesthetized cat. Cryoloops were placed over A1 and posterior auditory field (PAF). Multiunit neuronal responses to noise burst and tonal stimuli were recorded in DZ during cortical deactivation of each field individually and in concert. Deactivation of A1 suppressed peak neuronal responses in DZ regardless of stimulus and resulted in increased minimum thresholds and reduced absolute bandwidths for tone frequency receptive fields in DZ. PAF deactivation had less robust effects on DZ firing rates and receptive fields compared with A1 deactivation, and combined A1/PAF cooling was largely driven by the effects of A1 deactivation at the population level. These results provide physiological support for the current anatomically based model of both serial and parallel processing schemes in auditory cortical hierarchical organization.

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Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1203 ◽

2015 ◽

Vol 282 (1811) ◽

pp. 20151203 ◽

Cited By ~ 20

Author(s):

Gregory S. Berns ◽

Peter F. Cook ◽

Sean Foxley ◽

Saad Jbabdi ◽

Karla L. Miller ◽

...

Keyword(s):

Diffusion Tensor Imaging ◽

Auditory Cortex ◽

Auditory System ◽

Temporal Lobe ◽

Diffusion Tensor ◽

Primary Auditory Cortex ◽

Post Mortem ◽

Terrestrial Mammals ◽

Medial Geniculate ◽

Archival Specimens

The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of ‘associative′ regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin ( Delphinus delphis ) and a pantropical dolphin ( Stenella attenuata ) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.

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