Mismatch Responses in the Awake Rat: Evidence from Epidural Recordings of Auditory Cortical Fields

Jung, Fabienne; Stephan, Klaas Ε.; Backes, Heiko; Moran, Rosalyn J.; Gramer, Markus; Kumagai, Tetsuya; Graf, Rudolf; Endepols, Heike; Tittgemeyer, Marc

doi:10.1371/journal.pone.0063203

Cited by 37 publications

(57 citation statements)

References 57 publications

(72 reference statements)

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“…Furthermore, in the time window in which some auditory MMN responses were observed in the rat cortex (e.g. Jung et al ., ), we found no neuronal difference in the response rate between the sequence conditions. Thus, the response patterns observed in gerbil AC and IC neurons may contribute to MMN but are unlikely to be a representation of MMN.…”

Section: Discussionmentioning

confidence: 99%

Release from informational masking by auditory stream segregation: perception and its neural correlate

Dolležal

Tolnai

Beutelmann

et al. 2018

Eur J of Neuroscience

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In the analysis of acoustic scenes, we easily miss sounds or are insensitive to sound features that are salient if presented in isolation. This insensitivity that is not due to interference in the inner ear is termed informational masking (IM). So far, the cellular mechanisms underlying IM remained elusive. Here, we apply a sequential IM paradigm to humans and gerbils using a sound level increment detection task determining the sensitivity to target tones in a background of standard (same frequency) and distracting tones (varying in level and frequency). The amount of IM that was indicated by the level increment thresholds depended on the frequency separation between the distracting and the standard and target tones. In humans and gerbils, we observed similar perceptual thresholds. A release from IM of more than 20 dB was observed in both species if the distracting tones were well segregated in frequency from the other tones. Neuronal rate responses elicited by similar sequences in gerbil inferior colliculus and auditory cortex were recorded. At both levels of the auditory pathway, the neuronal thresholds obtained with a signal-detection-theoretic approach deducing the sensitivity from the analysis of the neurons' receiver operating characteristics matched the psychophysical thresholds revealing that IM already emerges at midbrain level. By applying objective response measures in physiology and psychophysics, we demonstrated that the population of neurons has a sufficient sensitivity for explaining the perceptual level increment thresholds indicating IM. There was a good correspondence between the neuronal and perceptual release from IM being related to auditory stream segregation.

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Section: Discussionmentioning

confidence: 99%

Release from informational masking by auditory stream segregation: perception and its neural correlate

Dolležal

Tolnai

Beutelmann

et al. 2018

Eur J of Neuroscience

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“…Thus, a starting point for elucidating how alterations in neurotransmission contribute to deficits in deviance detection is to employ animal models to pharmacologically isolate the role of specific modulatory substances on event-related potentials or on correlated neuronal activity. Recent studies have demonstrated that MMN-like responses occur in animal models like the rat (Harms et al, 2014;Jung et al, 2013). Likewise, neurons that exhibit a specific decrement in their response to repetitive but not to rare sounds have been characterized in animals.…”

Section: Overviewmentioning

confidence: 99%

Stimulus-specific adaptation in the inferior colliculus: The role of excitatory, inhibitory and modulatory inputs

Ayala

Pérez-González

Malmierca

2016

Biological Psychology

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Patients suffering from pathologies such as schizophrenia, depression or dementia exhibit cognitive impairments, some of which can be reflected in event-related potential (ERP) measurements as the mismatch negativity (MMN). The MMN is one of the most commonly used ERPs and provides an electrophysiological index of auditory change or deviance detection. Moreover, MMN has been positioned as a potentially promising biomarker candidate for the diagnosis and prediction of the outcome of schizophrenia. Dysfunction of neural receptors has been linked to the etiopathology of schizophrenia or the induction of psychophysiological anomalies similar to those observed in schizophrenia. Stimulus-specific adaptation (SSA) is a neural mechanism that contributes to the upstream processing of auditory change detection. Auditory neurons that exhibit SSA specifically adapt their response to repetitive sounds but maintain their excitability to respond to rare ones. Thus, by studying the role of neuronal receptors on SSA, we can contribute to detangle the cellular bases of the impairments in deviance processing occurring in mental pathologies. Here, we review the current knowledge on the effect of GABAA-mediated inhibition and the modulation of acetylcholine on SSA in the inferior colliculus, and we add unpublished original data obtained blocking glutamate receptors. We found that the blockade of GABAA and glutamate receptors mediates an overall increase or decrease of the neural response, respectively, while acetylcholine affects only the response to the repetitive sounds. These results demonstrate that GABAergic, glutamatergic and cholinergic receptors play different and complementary roles on shaping SSA.

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“…In addition, this issue is more controversial in rodent models because of considerable variation in data among studies, possibly due to variation of reference electrode position or anesthetic agents [36]–[45]. Thus, comprehensive experiments are still required to conclude how closely the putative MMN (MMNp) in animals meets the general characteristics of MMN in humans.…”

Section: Introductionmentioning

confidence: 99%

Cortical Mapping of Mismatch Negativity with Deviance Detection Property in Rat

2013

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Mismatch Negativity (MMN) is an N-methyl-d-aspartic acid (NMDA)-mediated, negative deflection in human auditory evoked potentials in response to a cognitively discriminable change. MMN-like responses have been extensively investigated in animal models, but the existence of MMN equivalent is still controversial. In this study, we aimed to investigate how closely the putative MMN (MMNp) in rats exhibited the comparable properties of human MMN. We used a surface microelectrode array with a grid of 10×7 recording sites within an area of 4.5×3.0 mm to densely map evoked potentials in the auditory cortex of anesthetized rats under the oddball paradigm. Firstly, like human MMN, deviant stimuli elicited negative deflections in auditory evoked potentials following the positive middle-latency response, termed P1. Secondly, MMNp exhibited deviance-detecting property, which could not be explained by simple stimulus specific adaptation (SSA). Thirdly, this MMNp occurred focally in the auditory cortex, including both the core and belt regions, while P1 activation focus was obtained in the core region, indicating that both P1 and MMNp are generated in the auditory cortex, yet the sources of these signals do not completely overlap. Fourthly, MMNp significantly decreased after the application of AP5 (D-(-)-2-amino-5-phosphonopentanoic acid), an antagonist at NMDA receptors. In stark contrast, AP5 affected neither P1 amplitude nor SSA of P1. These results provide compelling evidence that the MMNp we have examined in rats is functionally comparable to human MMN. The present work will stimulate translational research into MMN, which may help bridge the gap between electroencephalography (EEG)/magnetoencephalography (MEG) studies in humans and electrophysiological studies in animals.

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Mismatch Responses in the Awake Rat: Evidence from Epidural Recordings of Auditory Cortical Fields

Cited by 37 publications

References 57 publications

Release from informational masking by auditory stream segregation: perception and its neural correlate

Release from informational masking by auditory stream segregation: perception and its neural correlate

Stimulus-specific adaptation in the inferior colliculus: The role of excitatory, inhibitory and modulatory inputs

Cortical Mapping of Mismatch Negativity with Deviance Detection Property in Rat

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