Evoked brain responses are generated by feedback loops

Abstract

Neuronal responses to stimuli, measured electrophysiologically, unfold over several hundred milliseconds. Typically, they show characteristic waveforms with early and late components. It is thought that early or exogenous components reflect a perturbation of neuronal dynamics by sensory input bottom-up processing. Conversely, later, endogenous components have been ascribed to recurrent dynamics among hierarchically disposed cortical processing levels, top-down effects. Here, we show that evoked brain responses are generated by recurrent dynamics in cortical networks, and late components of event-related responses are mediated by backward connections. This evidence is furnished by dynamic causal modeling of mismatch responses, elicited in an oddball paradigm. We used the evidence for models with and without backward connections to assess their likelihood as a function of peristimulus time and show that backward connections are necessary to explain late components. Furthermore, we were able to quantify the contribution of backward connections to evoked responses and to source activity, again as a function of peristimulus time. These results link a generic feature of brain responses to changes in the sensorium and a key architectural component of functional anatomy; namely, backward connections are necessary for recurrent interactions among levels of cortical hierarchies. This is the theoretical cornerstone of most modern theories of perceptual inference and learning.connectivity ͉ dynamic causal modeling ͉ EEG ͉ predictive coding ͉ top-down E vent-related potentials (ERPs) or event-related fields (ERFs) in electroencephalography (EEG) and magnetoencephalography (MEG) are among the mainstays of noninvasive neuroscience. Typically, the response evoked by a stimulus evolves in a systematic way, showing a series of waves or components. Many of these components are elicited so reliably that they are studied in their own right. These include very early sensory-evoked potentials, observed within a few milliseconds; early cortical responses such as the N1 and P2 components; and later components expressed several hundred milliseconds afterward. Broadly speaking, ERP components can be divided into early and late (1). Early-or short-latency stimulus-dependent (exogenous) components reflect the integrity of primary afferent pathways. Late stimulus-independent (endogenous) components entail long-latency (Ͼ100 ms) responses thought to reflect cognitive processes (1, 2). Early components have been associated with exogenous bottom-up stimulus-bound effects, whereas late components have been ascribed to endogenous dynamics involving top-down influences. Indeed, the amplitude and latency of early (e.g., P1 and N1) and late (e.g., N2pc) components have been used as explicit indices of bottom-up and top-down processing, respectively (3). Here, we demonstrate that late components are mediated by recurrent interactions among remote cortical regions; specifically, we show that late components rest on backward extrinsic corticocortical c...

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