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• W3083517448 abstract "A better understanding of the mechanisms through which we perceive our sensory environment is vital for anaesthesiology and consciousness science. Through a pragmatic approach based on tracking afferent signals, we have gradually understood how sensory stimuli are processed from the peripheral sensor, through the peripheral nervous system, into the spinal cord, thalamus, and cerebral cortex. This sensibly heralded the classical, and still dominant, view of sensory processing that focuses on feedforward transmission of sensory information to generate representations of the world around us. Here, perception relies heavily on external inputs driving neural representations of basic stimulus features in lower-order areas of the nervous system. These representations are subsequently elaborated on in successive processing stages, resulting in increasingly abstract representations in higher order cortical regions. Although there is considerable evidence to support this model, it fails to explain many phenomena such as similar physical stimuli producing alternate conscious experiences or illusions,1Geisler W.S. Kersten D. Illusions, perception and bayes.Nat Neurosci. 2002; 5: 508-510Crossref PubMed Scopus (141) Google Scholar bistable perception,2Weilnhammer V. Stuke H. Hesselmann G. Sterzer P. Schmack K. A predictive coding account of bistable perception — a model-based fMRI study.PLoS Comput Biol. 2017; 13e1005536Crossref PubMed Scopus (38) Google Scholar,3Sanders R.D. Winston J.S. Barnes G.R. Rees G. Magnetoencephalographic correlates of perceptual state during auditory bistability.Sci Rep. 2018; 8: 976Crossref PubMed Scopus (5) Google Scholar or our ability to shape our own sensory perceptions (e.g. we can control our perception in illusions or use it to ‘fill in the blanks’, as in the McGurk effect4McGurk H. MacDonald J. Hearing lips and seeing voices.Nature. 1976; 264: 746-748Crossref PubMed Scopus (3678) Google Scholar (https://www.youtube.com/watch?v=2k8fHR9jKVM)). An alternative view is gaining traction, that is predictive coding. In the predictive coding model, higher order brain regions (such as frontal cortex) constantly generate and update hypotheses of the sensory world. These hypotheses are then matched to incoming sensory information, through descending/feedback projections that share these predictions with lower order areas of the sensory hierarchy. If the actual (observed) sensory stimuli do not match the predictions, a feedforward ‘prediction error’ is generated and propagated up the cortical hierarchy to update the higher order cortical prediction of the world.5Rao R.P. Ballard D.H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects.Nat Neurosci. 1999; 2: 79-87Crossref PubMed Scopus (2390) Google Scholar,6Bastos A.M. Usrey W.M. Adams R.A. Mangun G.R. Fries P. Friston K.J. Canonical microcircuits for predictive coding.Neuron. 2012; 76: 695-711Abstract Full Text Full Text PDF PubMed Scopus (1013) Google Scholar Depending on the reliability of the sensory evidence, the influence of prediction errors on model updating can be regulated, a concept known as precision. For example, under noisy conditions, prediction errors can be down weighted to avoid unnecessary model updates of the predictions. Such a role for modulating the gain of prediction errors has been proposed for the higher order thalamus, such as the pulvinar,7Kanai R. Komura Y. Shipp S. Friston K. Cerebral hierarchies: predictive processing, precision and the pulvinar.Philos Trans R Soc Lond B Biol Sci. 2015; 370: 20140169Crossref PubMed Scopus (151) Google Scholar which is extensively and reciprocally connected with the cortex, thus ideally positioned to regulate cortical gain.8Saalmann Y.B. Kastner S. Cognitive and perceptual functions of the visual thalamus.Neuron. 2011; 71: 209-223Abstract Full Text Full Text PDF PubMed Scopus (261) Google Scholar,9Saalmann Y.B. Pinsk M.A. Wang L. Li X. Kastner S. The pulvinar regulates information transmission between cortical areas based on attention demands.Science. 2012; 337: 753-756Crossref PubMed Scopus (530) Google Scholar An advantage of this model is that it accounts for how sensory processing can occur so rapidly and how illusions, or control of perception, is possible. Predictive coding also explains how we make predictions about our learned sensory environment, for example when we hear a siren, predict an emergency response vehicle and plan to move out of the way; this fits with the hierarchical (and reciprocal) connectivity of the cortex. Hence, given its behavioural relevance and neurophysiological basis, it seems a solid model for further understanding sensory perception. The clinical intent of anaesthesia is to ablate sensory perception,10Sanders R.D. Tononi G. Laureys S. Sleigh J.W. Unresponsiveness ≠ unconsciousness.Anesthesiology. 2012; 116: 946-959Crossref PubMed Scopus (244) Google Scholar what we refer to as sensory disconnection, and provide immobility and amnesia.11Eger 2nd, E.I. Sonner J.M. Anaesthesia defined (gentlemen, this is no humbug).Best Pract Res Clin Anaesthesiol. 2006; 20: 23-29Crossref PubMed Scopus (41) Google Scholar Owing to the intimate link between predictive coding and sensory processing, we argue that predictive coding provides a natural framework through which to study anaesthetic mechanisms. As anaesthetics dramatically disturb neurophysiological processes, it is reasonable to expect that predictive coding will be disturbed. We propose that the four critical elements of predictive coding may be differentially affected in different states of sensory disconnection, such as anaesthesia: (1) higher order cortex prediction generation, (2) feedback of predictions, (3) feedforward prediction error propagation, or (4) estimates of precision. We argue below that sensory disconnection (such as dreams during sleep or sedation/anaesthesia) results from perturbing elements (3), (4), or both; whereas unconsciousness (no experience) results from perturbing (1), (2), or both. In states of sensory disconnection,10Sanders R.D. Tononi G. Laureys S. Sleigh J.W. Unresponsiveness ≠ unconsciousness.Anesthesiology. 2012; 116: 946-959Crossref PubMed Scopus (244) Google Scholar we argue that there is an obvious mismatch between the predictions of the external world still being generated in some higher order cortical regions (e.g. ‘dreaming of lying on a beach’) and the actual sensory environment (a bedroom in the dead of night; Fig. 1). We propose that in sensory disconnection, the mismatch between the incoming sensory information and the generated model in higher order cortex (i.e. the dream) may be explained by impaired feedforward prediction error propagation, estimates of precision, or both (Fig. 1). As a consequence, the model in higher order cortex is not appropriately updated, and thus increasingly deviates from the external sensory environment, leading to disconnected and bizarre dreams. We propose that reductions in norepinephrine may be a critical mechanism of disconnection during sleep and anaesthesia10Sanders R.D. Tononi G. Laureys S. Sleigh J.W. Unresponsiveness ≠ unconsciousness.Anesthesiology. 2012; 116: 946-959Crossref PubMed Scopus (244) Google Scholar (which is supported by recent evidence12Hayat H. Regev N. Matosevich N. et al.Locus coeruleus norepinephrine activity mediates sensory-evoked awakenings from sleep.Sci Adv. 2020; 6 (eaaz4232)Crossref PubMed Scopus (24) Google Scholar). Similar ideas were articulated by Hobson and Friston13Hobson J.A. Friston K.J. Waking and dreaming consciousness: neurobiological and functional considerations.Prog Neurobiol. 2012; 98: 82-98Crossref PubMed Scopus (132) Google Scholar about rapid eye movement (REM) sleep, another state of sensory disconnection. Notably, these ideas yield testable hypotheses using sensory paradigms. Years of research have defined the feedforward pathways for differing sensory stimuli, allowing us to test measures of feedforward signalling. More recently, a critical role of higher order thalamic nuclei, such as the pulvinar, in weighting the trustworthiness of sensory evidence emerged.14Komura Y. Nikkuni A. Hirashima N. Uetake T. Miyamoto A. Responses of pulvinar neurons reflect a subject's confidence in visual categorization.Nat Neurosci. 2013; 16: 749-755Crossref PubMed Scopus (109) Google Scholar This weighting is akin to precision in the predictive coding nomenclature7Kanai R. Komura Y. Shipp S. Friston K. Cerebral hierarchies: predictive processing, precision and the pulvinar.Philos Trans R Soc Lond B Biol Sci. 2015; 370: 20140169Crossref PubMed Scopus (151) Google Scholar (Fig. 1). Thus, the predictive coding model provides clear neurophysiological hypotheses that may be tested to expedite discovery of the mechanisms of sensory disconnection. Some preliminary evidence supports the application of predictive coding theories to the study of sensory disconnection. For example, feedforward connectivity is diminished by propofol sedation,10Sanders R.D. Tononi G. Laureys S. Sleigh J.W. Unresponsiveness ≠ unconsciousness.Anesthesiology. 2012; 116: 946-959Crossref PubMed Scopus (244) Google Scholar suggesting that propagation of prediction error may be impaired. Reduced activity in the pulvinar nucleus during REM sleep (when the cortex was active)15Magnin M. Bastuji H. Garcia-Larrea L. Mauguiere F. Human thalamic medial pulvinar nucleus is not activated during paradoxical sleep.Cereb Cortex. 2004; 14: 858-862Crossref PubMed Scopus (31) Google Scholar fits with perturbed or diminished precision/weighting of external sensory evidence during (low norepinephrine) sleep-associated sensory disconnection given the role of pulvinar in precision, and its noradrenergic innervation. However, in these studies the conscious state of subjects was assumed and not confirmed. If the subjects were unconscious rather than dreaming, the investigators have studied additional mechanisms not necessary for sensory disconnection. In order to unravel the specific mechanisms of sensory disconnection, we need more thorough descriptors of the conscious state, perhaps through awakenings under sedation16Radek L. Kallionpaa R.E. Karvonen M. et al.Dreaming and awareness during dexmedetomidine- and propofol-induced unresponsiveness.Br J Anaesth. 2018; 121: 260-269Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar (and confirmed with the isolated forearm test17Gaskell A.L. Hight D.F. Winders J. et al.Frontal alpha–delta EEG does not preclude volitional response during anaesthesia: prospective cohort study of the isolated forearm technique.Br J Anaesth. 2017; 119: 664-673Abstract Full Text Full Text PDF PubMed Scopus (58) Google Scholar) combined with specific testing of sensory responses. Our interpretation of predictive coding allows us to make further inferences that would not be predicted by the feedforward model of sensory processing. Although we propose that feedforward signalling and weighting of sensory evidence is diminished in states of sensory disconnection, we suggest that there is mismatch between the feedback (higher order cortical) predictions and incoming sensory information (Fig. 1). The afferent subcortical sensory pathway from the peripheral sensor is relatively less affected by anaesthesia, allowing activation of primary sensory regions. However, the net increase in feedback to feedforward signalling leads to increases in activity in primary sensory cortex (increased prediction error signalling because of the mismatch in feedback:feedforward information). Although this may appear paradoxical, this explains an oft observed feature of sensory processing under anaesthesia, that of increased (or at least active) processing of sensory information in primary regions.18Plourde G. Belin P. Chartrand D. et al.Cortical processing of complex auditory stimuli during alterations of consciousness with the general anesthetic propofol.Anesthesiology. 2006; 104: 448-457Crossref PubMed Scopus (91) Google Scholar,19Banks M.I. Moran N.S. Krause B.M. Grady S.M. Uhlrich D.J. Manning K.A. Altered stimulus representation in rat auditory cortex is not causal for loss of consciousness under general anaesthesia.Br J Anaesth. 2018; 121: 605-615Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar We have observed diminished alpha power after transcranial magnetic stimulation in putative (but unconfirmed) states of disconnection of REM sleep and ketamine dissociative anaesthesia.20Darracq M. Funk C.M. Polyakov D. et al.Evoked alpha power is reduced in disconnected consciousness during sleep and anesthesia.Sci Rep. 2018; 8: 16664Crossref PubMed Scopus (8) Google Scholar As alpha oscillations are an index of neural excitability (low alpha power equals high activity and vice versa), we interpret this to mean there was increased excitability of cortex in states of sensory disconnection, consistent with the hypotheses mentioned above. We suspect (though it is unproven) that escalating doses of general anaesthetics make it more likely that subjects are unconscious rather than merely disconnected from the environment. Based on much earlier work, we hypothesise that this transition is accompanied by increased slow wave activity over the posterior cortex, and decreased feedback across frontoparietal regions10Sanders R.D. Tononi G. Laureys S. Sleigh J.W. Unresponsiveness ≠ unconsciousness.Anesthesiology. 2012; 116: 946-959Crossref PubMed Scopus (244) Google Scholar,21Alkire M.T. Hudetz A.G. Tononi G. Consciousness and anesthesia.Science. 2008; 322: 876-880Crossref PubMed Scopus (761) Google Scholar, 22Mashour G.A. Hudetz A.G. Bottom-up and top-down mechanisms of general anesthetics modulate different dimensions of consciousness.Front Neural Circuits. 2017; 11: 44Crossref PubMed Scopus (57) Google Scholar, 23Siclari F. Baird B. Perogamvros L. et al.The neural correlates of dreaming.Nat Neurosci. 2017; 20: 872-878Crossref PubMed Scopus (237) Google Scholar (Fig. 1). Our recent data support this notion24Redinbaugh M.J. Phillips J.M. Kambi N.A. et al.Thalamus modulates consciousness via layer-specific control of cortex.Neuron. 2020; 106: 66-75 e12Abstract Full Text Full Text PDF PubMed Scopus (57) Google Scholar; however, it is important to note that feedback connectivity is decreased in states where subjects remain conscious25Seymour R.A. Rippon G. Gooding-Williams G. Schoffelen J.M. Kessler K. Dysregulated oscillatory connectivity in the visual system in autism spectrum disorder.Brain. 2019; 142: 3294-3305Crossref PubMed Scopus (16) Google Scholar and so the degree to which feedback connectivity needs to be decreased to induce unconsciousness needs to be established. In sum, we consider that perturbations to higher order cortex (that generates predictions) and the feedback connections from those areas may be more important for inducing unconsciousness (Fig. 1). Indeed, based on recent data, posterior higher order cortical areas may be most critical for supporting the conscious state.26Koch C. Massimini M. Boly M. Tononi G. Neural correlates of consciousness: progress and problems.Nat Rev Neurosci. 2016; 17: 307-321Crossref PubMed Scopus (514) Google Scholar Understanding these mechanisms is important for two reasons: (1) monitoring the anaesthetic state and (2) design of anaesthetic regimens. Although improving the high standard of care for the prevention of explicit recall is extremely challenging,27Drummond J.C. Monitoring depth of anesthesia: with emphasis on the application of the bispectral index and the middle latency auditory evoked response to the prevention of recall.Anesthesiology. 2000; 93: 876-882Crossref PubMed Scopus (236) Google Scholar rates of responsiveness on the isolated forearm technique remain substantially higher than the low rates of recall,28Sanders R.D. Gaskell A. Raz A. et al.Incidence of connected consciousness after tracheal intubation: a prospective, international, multicenter cohort study of the isolated forearm technique.Anesthesiology. 2017; 126: 214-222Crossref PubMed Scopus (52) Google Scholar which is at odds with patient expectations about clinical anaesthesia.29Rowley P. Boncyk C. Gaskell A. et al.What do people expect of general anaesthesia?.Br J Anaesth. 2017; 118: 486-488Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar We need new approaches to depth of anaesthesia monitoring that go beyond preventing explicit recall. Alternatively, perhaps we can modify the way we provide anaesthesia through illuminating how we can modulate the mechanisms of predictive coding, and hence sensory perception. RDS and YBS are supported by National Institute of Health (USA) 1R01NS117901-01 . RDS is supported by National Institute of Health (USA) R01 AG063849-01 ." @default.
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• W3083517448 date "2021-01-01" @default.
• W3083517448 modified "2023-10-03" @default.
• W3083517448 title "Predictive coding as a model of sensory disconnection: relevance to anaesthetic mechanisms" @default.
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