Predictive coding as a model of sensory disconnection: relevance to anaesthetic mechanisms

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