Circular inferences in schizophrenia

Renaud Jardri, Sophie Denève
2013 Brain  
A considerable number of recent experimental and computational studies suggest that subtle impairments of excitatory to inhibitory balance or regulation are involved in many neurological and psychiatric conditions. The current paper aims to relate, specifically and quantitatively, excitatory to inhibitory imbalance with psychotic symptoms in schizophrenia. Considering that the brain constructs hierarchical causal models of the external world, we show that the failure to maintain the excitatory
more » ... ain the excitatory to inhibitory balance results in hallucinations as well as in the formation and subsequent consolidation of delusional beliefs. Indeed, the consequence of excitatory to inhibitory imbalance in a hierarchical neural network is equated to a pathological form of causal inference called 'circular belief propagation'. In circular belief propagation, bottom-up sensory information and top-down predictions are reverberated, i.e. prior beliefs are misinterpreted as sensory observations and vice versa. As a result, these predictions are counted multiple times. Circular inference explains the emergence of erroneous percepts, the patient's overconfidence when facing probabilistic choices, the learning of 'unshakable' causal relationships between unrelated events and a paradoxical immunity to perceptual illusions, which are all known to be associated with schizophrenia. Abbreviations: GABA = gamma-aminobutyric acid; LOR = log-odd ratio; NMDA = N-methyl-D-aspartate Although the exact underlying pathophysiological mechanisms for this disorder remain enigmatic, a substantial amount of physiological (Uhlhaas and Singer, 2010; Mulert et al., 2011) and postmortem (Lewis et al., 2005) evidence converges to suggest an impairment of gamma-aminobutyric acid (GABA) transmission or of N-methyl-D-aspartate (NMDA) receptor plasticity in schizophrenia (Stephan et al., 2009). These findings have contributed to a re-conceptualization of this disorder as a possible disruption in the neural excitatory to inhibitory balance (O'Donnell, 2011). Evidence of an excitatory to inhibitory imbalance in schizophrenia includes recent support for an alteration in the inhibitory GABAergic transmission of cortical microcircuits, comprising represented as 'nodes'. Arrows represent causal relationships. Sensory evidence is provided at the bottom and prior evidence at the top of the hierarchy. (B) Neural network that implements causal inference in this toy example. M xy represents the message sent by node x to node y. The overall flow of messages in the network is under the control of inhibitory loops (yellow lines: feed-forward connections; blue lines: feedback connections; green circles: upward inhibitory loops; black circles: downward inhibitory loops). (C) Belief propagation in the intact and impaired networks. Left: normal network that performs belief propagation. Because of intact inhibitory loops, ascending messages that correspond to sensory likelihoods (magenta) and descending messages that correspond to prior expectations (violet) are propagated only once in each direction, appropriately sharing prior and sensory information among all of the neurons. Right: impaired network without inhibitory loops. Top-down and bottom-up messages are uncontrollably propagated multiple times in each direction, which results in the multiple overcounting of the same redundant sensory and prior information. (D) Consequences of circular belief propagation. The belief obtained through iterating the network dynamics is out of proportion with the available sensory and prior evidence. This construct results in overconfidence (i.e. probabilities only slightly above 0.5 are perceived as being close to 1, and probabilities just below 0.5 are perceived as being close to zero). Circular inferences in schizophrenia Brain 2013: 136; 3227-3241 | 3229
doi:10.1093/brain/awt257 pmid:24065721 fatcat:dosfdluribfdzbt4dp3gsm34he