Indexing sensory plasticity: Evidence for distinct Predictive Coding and Hebbian learning mechanisms in the cerebral cortex

Abstract

The Roving Mismatch Negativity (MMN), and Visual LTP paradigms are widely used as independent measures of sensory plasticity. However, the paradigms are built upon fundamentally different (and seemingly opposing) models of perceptual learning; namely, Predictive Coding (MMN) and Hebbian plasticity (LTP). The aim of the current study was to compare the generative mechanisms of the MMN and visual LTP, therefore assessing whether Predictive Coding and Hebbian mechanisms co-occur in the brain. Forty participants were presented with both paradigms during EEG recording. Consistent with Predictive Coding and Hebbian predictions, Dynamic Causal Modelling revealed that the generation of the MMN modulates forward and backward connections in the underlying network, while visual LTP only modulates forward connections. These results suggest that both Predictive Coding and Hebbian mechanisms are utilized by the brain under different task demands. This therefore indicates that both tasks provide unique insight into plasticity mechanisms, which has important implications for future studies of aberrant plasticity in clinical populations.

Human sensory Long-Term Potentiation (LTP) predicts visual memory performance and is modulated by the brain-derived neurotrophic factor (BDNF) Val66Met polymorphism

“…First presented by Teyler et al, 11 , the sensory LTP paradigm typically involves presenting participants with high-frequency (~9Hz) visual stimulation, which leads to an enhancement of the visually-evoked potential (VEP) to subsequent low-frequency (~1Hz) presentations of the same stimulus. This enhancement has been shown to conform to many of the Hebbian characteristics of LTP [12][13][14] , and is generated 4 by a bottom-up modulation of connection strength between occipital and temporal regions 15 .…”

Modelling thalamocortical circuitry shows visually induced LTP changes laminar connectivity in human visual cortex

“…The purpose of the ERP analysis was to confirm modulation of the ERP had occurred and so was conducted solely to demonstrate evidence of VEP modulation post-tetanus. As in previous studies an occipito-parietal ROI was employed, comprising the following electrodes: P1, P2, P3, P4, P5, P6, P7, P8, Pz, PO3, PO4, PO7, PO8, PO9, PO10, POz, O1, O2, and Oz (Spriggs et al, 2018;Sumner, McMilllan, et al, 2018). A 3-way repeated measures ANOVA was implemented across a 250 ms time window.…”

“…Source analysis revealed a significant effect of photic tetanus that was particularly strong in visual cortex. As the main peaks were in calcarine fissure and yet the effect of visual LTP has been most typically studied in extrastriate cortex Spriggs et al, 2018;Sumner, Spriggs, et al, 2018a;Sumner et al, 2020;Teyler et al, 2005), a peak in left middle occipital gyrus (MOG) was selected from the literature (Spriggs et al, 2018) that was still within the significant area of activation for the current study: MNI [-36, -90, 4].…”

“…Connectivity changes associated with the visual LTP paradigm have been assessed using DCM and an adapted, simple Jansen and Rit (1995) neural mass model for evoked-potential research. To construct these networks, the sources typically associated with the induced LTP related change include greater activation in the extrastriate visual cortex, dorsal and ventral visual streams, and frontal cortex (Spriggs et al, 2018;Sumner et al, 2020;Sumner, Spriggs, et al, 2018b). As a result of Hebbian plasticity changes, modulation of excitatory forward projecting connections, as well as local modulation of the cortical microcircuit has been replicated (Spriggs et al, 2018;Sumner et al, 2020;Sumner, Spriggs, et al, 2018b).…”

“…To construct these networks, the sources typically associated with the induced LTP related change include greater activation in the extrastriate visual cortex, dorsal and ventral visual streams, and frontal cortex (Spriggs et al, 2018;Sumner et al, 2020;Sumner, Spriggs, et al, 2018b). As a result of Hebbian plasticity changes, modulation of excitatory forward projecting connections, as well as local modulation of the cortical microcircuit has been replicated (Spriggs et al, 2018;Sumner et al, 2020;Sumner, Spriggs, et al, 2018b). However, there is a lack of rodent research on the impact of LTP on cortico-cortical network connectivity to allow for detailed inference on the nature of resulting changes.…”