scholarly journals Learning of complex auditory patterns changes intrinsic and feedforward effective connectivity between Heschl’s gyrus and planum temporale

2019 ◽  
Author(s):  
Massimo Lumaca ◽  
Martin J. Dietz ◽  
Niels Chr. Hansen ◽  
David R. Quiroga-Martinez ◽  
Peter Vuust

AbstractLearning of complex auditory sequences such as language and music can be thought of as the continuous optimisation of internal predictive representations of sound-pattern regularities, driven by prediction errors. In predictive coding (PC), this occurs through changes in the intrinsic and extrinsic connectivity of the relevant cortical networks, whereby minimization of precision-weighted prediction error signals improves the accuracy of future predictions. Here, we employed Dynamic Causal Modelling (DCM) on functional magnetic resonance (fMRI) data acquired during the presentation of complex auditory patterns. In an oddball paradigm, we presented 52 volunteers (non-musicians) with isochronous 5-tone melodic patterns (standards), randomly interleaved with rare novel patterns comprising contour or pitch interval changes (deviants). Here, listeners must update their standard melodic models whenever they encounter unexpected deviant stimuli. Contour deviants induced an increased BOLD response, as compared to standards, in primary (Heschl’s gyrus, HG) and secondary auditory cortices (planum temporale, PT). Within this network, we found a left-lateralized increase in feedforward connectivity from HG to PT for deviant responses and a concomitant disinhibition within left HG. Consistent with PC, our results suggest that model updating in auditory pattern perception and learning is associated with specific changes in the excitatory feedforward connections encoding prediction errors and in the intrinsic connections that encode the precision of these errors and modulate their gain.Significance statementThe learning of complex auditory stimuli such as music and speech can be thought of as the continuous optimisation of brain predictive models driven by prediction errors. Using dynamic causal modelling on fMRI data acquired during a melodic oddball paradigm, we here show that brain responses to unexpected sounds were best explained by an increase in excitation within Heschl’s gyrus and an increase in forward connections from Heschl’s gyrus to planum temporale. Our results are consistent with a predictive coding account of sensory learning, whereby prediction error responses to new sounds drive model adjustments via feedforward connections and intrinsic connections encode the confidence of these prediction errors.

2020 ◽  
Vol 32 (1) ◽  
pp. 124-140 ◽  
Author(s):  
Hyojeong Kim ◽  
Margaret L. Schlichting ◽  
Alison R. Preston ◽  
Jarrod A. Lewis-Peacock

The human brain constantly anticipates the future based on memories of the past. Encountering a familiar situation reactivates memory of previous encounters, which can trigger a prediction of what comes next to facilitate responsiveness. However, a prediction error can lead to pruning of the offending memory, a process that weakens its representation in the brain and leads to forgetting. Our goal in this study was to evaluate whether memories are spared from such pruning in situations that allow for accurate predictions at the categorical level, despite prediction errors at the item level. Participants viewed a sequence of objects, some of which reappeared multiple times (“cues”), followed always by novel items. Half of the cues were followed by new items from different (unpredictable) categories, while others were followed by new items from a single (predictable) category. Pattern classification of fMRI data was used to identify category-specific predictions after each cue. Pruning was observed only in unpredictable contexts, while encoding of new items was less robust in predictable contexts. These findings demonstrate that how associative memories are updated is influenced by the reliability of abstract-level predictions in familiar contexts.


NeuroImage ◽  
2012 ◽  
Vol 62 (1) ◽  
pp. 464-481 ◽  
Author(s):  
J. Daunizeau ◽  
K.E. Stephan ◽  
K.J. Friston

Brain ◽  
2021 ◽  
Author(s):  
Natalie E Adams ◽  
Laura E Hughes ◽  
Matthew A Rouse ◽  
Holly N Phillips ◽  
Alexander D Shaw ◽  
...  

Abstract The clinical syndromes caused by frontotemporal lobar degeneration are heterogeneous, including the behavioural variant frontotemporal dementia (bvFTD) and progressive supranuclear palsy (PSP). Although pathologically distinct, they share many behavioural, cognitive and physiological features, which may in part arise from common deficits of major neurotransmitters such as γ-aminobutyric acid (GABA). Here, we quantify the GABA-ergic impairment and its restoration with dynamic causal modelling of a double-blind placebo-controlled crossover pharmaco-magnetoencephalography study. We analysed 17 people with bvFTD, 15 people with progressive supranuclear palsy, and 20 healthy age- and gender-matched controls. In addition to neuropsychological assessment and structural magnetic resonance imaging, participants undertook two magnetoencephalography sessions using a roving auditory oddball paradigm: Once on placebo and once on 10 mg of the oral GABA reuptake inhibitor tiagabine. A subgroup underwent ultrahigh-field magnetic resonance spectroscopy measurement of GABA concentration, which was reduced among patients. We identified deficits in frontotemporal processing using conductance-based biophysical models of local and global neuronal networks. The clinical relevance of this physiological deficit is indicated by the correlation between top-down connectivity from frontal to temporal cortex and clinical measures of cognitive and behavioural change. A critical validation of the biophysical modelling approach was evidence from Parametric Empirical Bayes analysis that GABA levels in patients, measured by spectroscopy, were related to posterior estimates of patients’ GABA-ergic synaptic connectivity. Further evidence for the role of GABA in frontotemporal lobar degeneration came from confirmation that the effects of tiagabine on local circuits depended not only on participant group, but also on individual baseline GABA levels. Specifically, the phasic inhibition of deep cortico-cortical pyramidal neurons following Tiagabine, but not placebo, was a function of GABA concentration. The study provides proof-of-concept for the potential of dynamic causal modelling to elucidate mechanisms of human neurodegenerative disease, and explain the variation in response to candidate therapies among patients. The laminar- and neurotransmitter-specific features of the modelling framework, can be used to study other treatment approaches and disorders. In the context of frontotemporal lobar degeneration, we suggest that neurophysiological restoration in selected patients, by targeting neurotransmitter deficits, could be used to bridge between clinical and preclinical models of disease, and inform the personalised selection of drugs and stratification of patients for future clinical trials.


2020 ◽  
Author(s):  
Andreas Strube ◽  
Michael Rose ◽  
Christian Büchel

In the context of a generative model, such as predictive coding, pain perception can be construed as the integration of expectation and nociceptive input with their difference denoted as a prediction error. In a previous neuroimaging study (Geuter et al., 2017) we observed an important role of the insula in such a model, but could not establish its temporal aspects. Here we employed electroencephalography to investigate neural representations of predictions and prediction errors in heat pain processing. Our data show that alpha-to-beta activity was associated with pain expectation, followed by gamma band activity associated with absolute prediction errors. Source reconstruction revealed the insula as a common region for both effects. This temporal sequence of expectation related alpha-to-beta activity, followed by prediction error associated gamma activity in the insula, provides a possible mechanisms for the temporal integrating of pain predictions and prediction errors in the context of a generative model.


2021 ◽  
Author(s):  
Roshini Randeniya ◽  
Jason B Mattingley ◽  
Marta Garrido

Bayesian models of autism suggest that disruptions in context-sensitive prediction error weighting may underpin sensory perceptual alterations, such as hypersensitivities. We used an auditory oddball paradigm with pure tones arising from high or low uncertainity contexts to determine whether autistic individuals display differences in context adjustment relative to neurotypicals. We did not find group differences in early prediction error responses indexed by mismatch negativity. However, the autism group had larger evoked responses to outliers, at 300ms latency suggesting a greater reorienting of attention to surprising sounds. A dimensional approach revealed a positive correlation between context-dependent prediction errors and auditory sensitivities, but not with autistic traits. These findings suggest that autism studies may benefit from accounting for sensory sensitivities in group comparisons.


2021 ◽  
Author(s):  
David Ricardo Quiroga-Martinez ◽  
Krzysztof Basinski ◽  
Jonathan Nasielski ◽  
Barbara Tillmann ◽  
Elvira Brattico ◽  
...  

Many natural sounds have frequency spectra composed of integer multiples of a fundamental frequency. This property, known as harmonicity, plays an important role in auditory information processing. However, the extent to which harmonicity influences the processing of sound features beyond pitch is still unclear. This is interesting because harmonic sounds have lower information entropy than inharmonic sounds. According to predictive processing accounts of perception, this property could produce more salient neural responses due to the brain weighting of sensory signals according to their uncertainty. In the present study, we used electroencephalography to investigate brain responses to harmonic and inharmonic sounds commonly occurring in music: piano tones and hi-hat cymbal sounds. In a multi-feature oddball paradigm, we measured mismatch negativity (MMN) and P3a responses to timbre, intensity, and location deviants in listeners with and without congenital amusia, an impairment of pitch processing. As hypothesized, we observed larger amplitudes and earlier latencies for harmonic compared to inharmonic sounds for both MMN and P3a responses. These harmonicity effects were modulated by sound feature. Moreover, the difference in P3a latency between harmonic and inharmonic sounds was larger for controls than amusics. We propose an explanation of these results based on predictive coding and discuss the relationship between harmonicity, information entropy, and precision weighting of prediction errors.


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