Cellular mechanisms of cooperative context-sensitive predictive inference

• Published in: Current research in neurobiology Vol. 6; p. 100129
• Main Authors: Marvan, Tomáš, Phillips, William A.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.01.2024; Elsevier
• Subjects: Apical amplification; Coherent Infomax; from the special issue: How Expectation Transforms Neural Representations and Perception, edited by Kerry Walker and Christopher I. Petkov; perceptual inference; prediction error minimisation; predictive coding; Apical amplification; predictive coding; Coherent Infomax; prediction error minimisation; perceptual inference
• ISSN: 2665-945X; 2665-945X
• DOI: 10.1016/j.crneur.2024.100129

We argue that prediction success maximization is a basic objective of cognition and cortex, that it is compatible with but distinct from prediction error minimization, that neither objective requires subtractive coding, that there is clear neurobiological evidence for the amplification of predicted signals, and that we are unconvinced by evidence proposed in support of subtractive coding. We outline recent discoveries showing that pyramidal cells on which our cognitive capabilities depend usually transmit information about input to their basal dendrites and amplify that transmission when input to their distal apical dendrites provides a context that agrees with the feedforward basal input in that both are depolarizing, i.e., both are excitatory rather than inhibitory. Though these intracellular discoveries require a level of technical expertise that is beyond the current abilities of most neuroscience labs, they are not controversial and acclaimed as groundbreaking. We note that this cellular cooperative context-sensitivity greatly enhances the cognitive capabilities of the mammalian neocortex, and that much remains to be discovered concerning its evolution, development, and pathology. A sketch of a context-sensitive pyramidal cell and its (dis) inhibitory regulation. The idealized diagram of a pyramidal cell shown on the left is adapted from Larkum and Phillips (2016). In the modulatory mode of operation, contextual input, which comes from diverse sources, amplifies transmission of information from the cell’s RF, i.e., the specific set of feedforward sources to which the cell is selectively sensitive. Ih: hyperpolarization activated current flow through HCN ion channels. AIZ: apical integration zone. FF: Feedforward. SIZ: somatic integration zone. IINs: four classes of inhibitory interneuron, i.e., PV, SST, VIP, and NGF. The output of NGF cells is shown in a highlighted form and without a well-specified target because they inhibit nearby pyramidal cells and IINs via volume release of GABA mainly in the upper layers, but also to a lesser extent in deeper layers. [Display omitted] •Prediction success maximization is a basic objective of cognition and cortex; it is compatible with but distinct from prediction error minimization.•Neither of these two objectives requires prediction error coding.•There is a clear neurobiological evidence for the amplification of predicted signals.•Pyramidal cells transmit information about input to their basal dendrites and amplify that transmission when input to their distal apical dendrites provides a context.