Evoked brain responses are generated by feedback loops

Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 01/2008; 104(52):20961-6. DOI: 10.1073/pnas.0706274105
Source: PubMed


Neuronal responses to stimuli, measured electrophysiologically, unfold over several hundred milliseconds. Typically, they show characteristic waveforms with early and late components. It is thought that early or exogenous components reflect a perturbation of neuronal dynamics by sensory input bottom-up processing. Conversely, later, endogenous components have been ascribed to recurrent dynamics among hierarchically disposed cortical processing levels, top-down effects. Here, we show that evoked brain responses are generated by recurrent dynamics in cortical networks, and late components of event-related responses are mediated by backward connections. This evidence is furnished by dynamic causal modeling of mismatch responses, elicited in an oddball paradigm. We used the evidence for models with and without backward connections to assess their likelihood as a function of peristimulus time and show that backward connections are necessary to explain late components. Furthermore, we were able to quantify the contribution of backward connections to evoked responses and to source activity, again as a function of peristimulus time. These results link a generic feature of brain responses to changes in the sensorium and a key architectural component of functional anatomy; namely, backward connections are necessary for recurrent interactions among levels of cortical hierarchies. This is the theoretical cornerstone of most modern theories of perceptual inference and learning.

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Available from: Marta I Garrido, Oct 13, 2015
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    • "Here, we test sensitivity and specificity of the synaptic ion channel inferences available through electrophysiological DCM, utilizing data from two cases of single-gene mutation channelopathies. In order to test these particular patients we augmented a conductance-based neural mass model (Moran et al., 2011c) of regionally specific sources (Garrido et al., 2007) to include ligand-gated sodium, calcium, and chloride channels — as well as voltage-gated potassium and calcium channels (Fig. 1). This augmented model was used to explain auditoryevoked ERFs produced by 94 healthy control participants and 2 patients with known mutations causing loss-of-function in the inward-rectifying potassium channel gene KCNJ2 and in the voltage-gated presynaptic calcium channel gene CACNA1A. "
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    ABSTRACT: Clinical assessments of brain function rely upon visual inspection of electroencephalographic waveform abnormalities in tandem with functional magnetic resonance imaging. However, no current technology proffers in vivo assessments of activity at synapses, receptors and ion-channels, the basis of neuronal communication. Using dynamic causal modeling we compared electrophysiological responses from two patients with distinct monogenic ion channelopathies and a large cohort of healthy controls to demonstrate the feasibility of assaying synaptic-level channel communication non-invasively. Synaptic channel abnormality was identified in both patients (100% sensitivity) with assay specificity above 89%, furnishing estimates of neurotransmitter and voltage-gated ion throughput of sodium, calcium, chloride and potassium. This performance indicates a potential novel application as an adjunct for clinical assessments in neurological and psychiatric settings. More broadly, these findings indicate that biophysical models of synaptic channels can be estimated non-invasively, having important implications for advancing human neuroimaging to the level of non-invasive ion channel assays. Copyright © 2015. Published by Elsevier Inc.
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    • "However, this more sophisticated approach is based upon the reconstruction of source activity underlying ERP components: if the P3 does not count as an NCC because it can also be elicited by subliminal stimuli (Reuter et al. 1989; Shevrin 2001), then it would seem that its DCM source and connectivity reconstruction (i.e., a mathematical transformation of the same data, plus several assumptions) cannot be an NCC either. This holds as well for ERP responses later than the P3, including the N400 modulated by semantic priming (Kiefer 2002; more below), that are predicted by Garrido et al. (2007) to involve top-down processing. Suppose, however, one could remove ERPs from the picture. "
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    DESCRIPTION: Recently, a number of neuroimaging studies have been conducted, aimed at detecting signs of consciousness in patients with a diagnosis of vegetative or minimally conscious state. The contributions appeared during an ongoing international ethical and socio-legal debate, on the admissibility of decisions to withdraw artificial nutrition from vegetative patients, thereby allowing them to die. We argue that neuroimaging is more likely to contribute to medical diagnosis and decision making if two requirements are met. First, those studies inferred awareness from the neural correlates of cognitive processes that are assumed to involve consciousness. However, neural correlates of consciousness proper, as defined by current philosophy and neuroscience, are the only admissible non-behavioral signs of awareness. Second, in those studies patients attempted to answer medically irrelevant questions by modulating their cortical activity in imagery tasks. We suggest patients should instead be queried on matters relevant to their clinical condition and quality of life.
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    • "This finding contrasts with the interpretation of these potentials as objective pain intensity markers, suggesting that the magnitude of the N2 response cannot be considered a direct read-out of pain intensity (Bromm and Lorenz, 1998), but rather reflects a complex pain-related process integrating stimulus salience and cognitive expectations (e.g., Legrain et al., 2011). This pattern of N2 potentials fits with recent evidence that both sensory prediction errors conveyed by forward connections and top-down predictions conveyed by backward connections are implicated in the generation of late cortical ERPs (N100 ms) (Garrido et al., 2007). For example, when a subject expects to have less pain (inhibitory mental imagery), but actually receive a painful stimulus, this would produce a net positive pain prediction error. "
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    ABSTRACT: Mental imagery has the potential to influence perception by directly altering sensory, cognitive, and affective brain activity associated with imagined content. While it is well established that mental imagery can both exacerbate and alleviate acute and chronic pain, it is currently unknown how imagery mechanisms regulate pain perception. For example, studies to date have been unable to determine whether imagery effects depend upon a general redirection of attention away from pain or related focused attentional mechanisms. To address these issues, we recorded subjective, behavioral and ERP responses using 64-channel EEG while healthy human participants applied a mental imagery strategy to decrease or increase pain sensations. When imagining a glove covering the forearm, participants reported decreased perceived intensity and unpleasantness, classified fewer high-intensity stimuli as painful, and showed a more conservative response bias. In contrast, when imagining a lesion on the forearm, participants reported increased pain intensity and unpleasantness, classified more low-intensity stimuli as painful, and displayed a more liberal response bias. Using a mass-univariate approach, we further showed differential modulation of the N2 potentials across conditions, with inhibition and facilitation respectively increasing and decreasing N2 amplitudes between 122 and 180 ms. Within this time window, source localization associated inhibiting vs. facilitating pain with neural activity in cortical regions involved in cognitive inhibitory control and in the retrieval of semantic information (i.e., right inferior frontal and temporal regions). In contrast, the main sources of neural activity associated with facilitating vs. inhibiting pain were identified in cortical regions typically implicated in salience processing and emotion regulation (i.e., left insular, inferior-middle frontal, supplementary motor and precentral regions). Overall, these findings suggest that the content of a mental image directly alters pain-related decision and evaluative processing to flexibly produce hypoalgesic and hyperalgesic outcomes. Copyright © 2015. Published by Elsevier Inc.
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