Deviance detection in auditory subcortical structures: what can we learn from neurochemistry and neural connectivity?

Duque, Daniel; Ayala, Yaneri A.; Malmierca, Manuel S.

doi:10.1007/s00441-015-2134-7

Cited by 20 publications

(17 citation statements)

References 265 publications

(295 reference statements)

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“…Our fMRI data show that cortical change-induced activity was accompanied by substantial subcortical activations, covering large portions of the thalamus as well as parts of the superior and inferior colliculi. These findings agree with previous studies reporting deviance-related processing at subcortical level, in particular in the inferior colliculus and the medial geniculate nucleus of the thalamus [Antunes and Malmierca, 2014;Cacciaglia et al, 2015;Duque et al, 2015;Mitchell et al, 2015;Slabu et al, 2012]. In animals, subcortical effects have been shown to occur earlier than on the cortical level, but to be modulated by corticofugal auditory cortex projections [Antunes and Malmierca, 2014;Antunes et al, 2010;Malmierca et al, 2009].…”

Section: Activation Spread Of Change-induced Activity Following Initisupporting

confidence: 92%

Mapping the spatiotemporal dynamics of processing task‐relevant and task‐irrelevant sound feature changes using concurrent EEG‐fMRI

Puschmann

Huster

Thiel

2016

Human Brain Mapping

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The cortical processing of changes in auditory input involves auditory sensory regions as well as different frontoparietal brain networks. The spatiotemporal dynamics of the activation spread across these networks has, however, not been investigated in detail so far. We here approached this issue using concurrent functional magnetic resonance imaging (fMRI) and electroencephalography (EEG), providing us with simultaneous information on both the spatial and temporal patterns of change‐related activity. We applied an auditory stimulus categorization task with switching categorization rules, allowing to analyze change‐related responses as a function of the changing sound feature (pitch or duration) and the task relevance of the change. Our data show the successive progression of change‐related activity from regions involved in early change detection to the ventral and dorsal attention networks, and finally the central executive network. While early change detection was found to recruit feature‐specific networks involving auditory sensory but also frontal and parietal brain regions, the later spread of activity across the frontoparietal attention and executive networks was largely independent of the changing sound feature, suggesting the existence of a general feature‐independent processing pathway of change‐related information. Task relevance did not modulate early auditory sensory processing, but was mainly found to affect processing in frontal brain regions. Hum Brain Mapp 37:3400–3416, 2016. © 2016 Wiley Periodicals, Inc.

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Section: Activation Spread Of Change-induced Activity Following Initisupporting

confidence: 92%

Mapping the spatiotemporal dynamics of processing task‐relevant and task‐irrelevant sound feature changes using concurrent EEG‐fMRI

Puschmann

Huster

Thiel

2016

Human Brain Mapping

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“…In addition to the convergence of depressing synapses that convey frequency-specific inputs, our model also incorporates surrounding inhibition. Broadly tuned neurons exhibited more extensive suppression and larger SSA strength (Figure 5 ), which is consistent with the stronger SSA found in the non-lemniscal pathway in which neurons have broader tunings (Malmierca et al, 2009 ; Duque et al, 2012 , 2015 ; Ayala and Malmierca, 2013 ; Ayala et al, 2015b ). This result implies that broadly tuned neurons might undergo more prominent adaptation due to broader convergence of inputs, including those from the CNIC or cortical feedback that cannot be fully covered by the present model (Ayala et al, 2015b ).…”

Section: Discussionsupporting

confidence: 78%

“…It is not generated by the corticocollicular projection through top-down modulation (Anderson and Malmierca, 2013 ; Malmierca et al, 2015 ). The predictive power of our model suggests that frequency-specific adaptation may be generated via a feedforward network, employing synaptic depression (Duque et al, 2015 ) of the afferents either from CNIC to cortical IC neurons or from a lower nucleus to CNIC. It is a variant of the adaptation of narrowly tuned modules (ANTM) model (Nelken, 2014 ), which was proposed previously (Mill et al, 2011a , b , 2012 ; Taaseh et al, 2011 ; Hershenhoren et al, 2014 ).…”

Section: Discussionmentioning

confidence: 95%

Frequency-specific adaptation and its underlying circuit model in the auditory midbrain

Shen

Zhao

Hong

2015

Front. Neural Circuits

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Receptive fields of sensory neurons are considered to be dynamic and depend on the stimulus history. In the auditory system, evidence of dynamic frequency-receptive fields has been found following stimulus-specific adaptation (SSA). However, the underlying mechanism and circuitry of SSA have not been fully elucidated. Here, we studied how frequency-receptive fields of neurons in rat inferior colliculus (IC) changed when exposed to a biased tone sequence. Pure tone with one specific frequency (adaptor) was presented markedly more often than others. The adapted tuning was compared with the original tuning measured with an unbiased sequence. We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency. Central adaptors elicited strong suppressive and repulsive changes while flank adaptors induced facilitative and attractive changes. Moreover, we proposed a two-layer model of the underlying network, which not only reproduced the adaptive changes in the receptive fields but also predicted novelty responses to oddball sequences. These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

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“…Hence, multiple excitatory, inhibitory and modulatory inputs converge onto single IC neurons (Ito & Oliver, 2010 that also receive neuromodulatory inputs from multiple sources (for a review, see Duque, Ayala, & Malmierca, 2015).…”

Section: Excitatory Inhibitory and Cholinergic Inputs To The Icmentioning

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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Deviance detection in auditory subcortical structures: what can we learn from neurochemistry and neural connectivity?

Cited by 20 publications

References 265 publications

Mapping the spatiotemporal dynamics of processing task‐relevant and task‐irrelevant sound feature changes using concurrent EEG‐fMRI

Mapping the spatiotemporal dynamics of processing task‐relevant and task‐irrelevant sound feature changes using concurrent EEG‐fMRI

Frequency-specific adaptation and its underlying circuit model in the auditory midbrain

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

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