The Cumulative Effects of Predictability on Synaptic Gain in the Auditory Processing Stream

Abstract

Stimulus predictability can lead to substantial modulations of brain activity, such as shifts in sustained magnetic field amplitude, measured with magnetoencephalography (MEG). Here, we provide a mechanistic explanation of these effects using MEG data acquired from healthy human volunteers (N = 13, 7 female). In a source-level analysis of induced responses, we established the effects of orthogonal predictability manipulations of rapid tone-pip sequences (namely, sequence regularity and alphabet size) along the auditory processing stream. In auditory cortex, regular sequences with smaller alphabets induced greater gamma activity. Furthermore, sequence regularity shifted induced activity in frontal regions toward higher frequencies. To model these effects in terms of the underlying neurophysiology, we used dynamic causal modeling for cross-spectral density and estimated slow fluctuations in neural (postsynaptic) gain. Using the model-based parameters, we accurately explain the sensor-level sustained field amplitude, demonstrating that slow changes in synaptic efficacy, combined with sustained sensory input, can result in profound and sustained effects on neural responses to predictable sensory streams.SIGNIFICANCE STATEMENT Brain activity can be strongly modulated by the predictability of stimuli it is currently processing. An example of such a modulation is a shift in sustained magnetic field amplitude, measured with magnetoencephalography. Here, we provide a mechanistic explanation of these effects. First, we establish the oscillatory neural correlates of independent predictability manipulations in hierarchically distinct areas of the auditory processing stream. Next, we use a biophysically realistic computational model to explain these effects in terms of the underlying neurophysiology. Finally, using the model-based parameters describing neural gain modulation, we can explain the previously unexplained effects observed at the sensor level. This demonstrates that slow modulations of synaptic gain can result in profound and sustained effects on neural activity.

Audio-visual combination of syllables involves time-sensitive dynamics following from fusion failure

“…Importantly, we observed that the temporal asynchrony effect in the IFG was followed by a similar effect in PAC, a finding that fits well with the observation that regularity in tone sequences modulates IFG activity, and that the estimated intervals propagate from the IFG to PAC 38,39 . Overall, our study confirm that the IFG originates descending signals about estimated precision or predictability of the sensory stimuli 64 .…”

“…Confirming recent literature, temporal asynchrony was reflected positively first in the IFG (20 ms pre-to 200 ms post-auditory stimulus onset), and then in PAC (around 300 ms postauditory stimulus onset) ( Figure 6). The sequence of positive coefficients in the IFG and then in PAC speaks to the role of the IFG in contextualising the sensory integration process 38,39 . shown in other studies 37 .…”

Evaluating the neurophysiological evidence for predictive processing as a model of perception

“…A particularly perplexing set of results in this literature comes from a series of studies reporting that the transition from random to regular sequences of auditory stimuli is accompanied by a sustained increase in neural activity measured with MEG, EEG, and fMRI, 144,154,155 in stark contrast to ES studies showing dampened neural responses to predictable stimuli. 78,81,156,157 One interpretation of this result is that the enhanced activity reflects the high precision-weighting afforded to low variance input.…”

“…78,81,156,157 One interpretation of this result is that the enhanced activity reflects the high precision-weighting afforded to low variance input. 155 However, since precision-weighting is applied to error units, this explanation of the sustained error signals rests upon the assumption that the increased precision more than compensates for the reduction in prediction error that would be expected over the course of exposure to a repeating, and therefore highly predictable, pattern of tones.…”

“…Although there is evidence that the predictability of a stimulus modulates activity in low-level sensory areas 103,128 and alters the functional connectivity between neural regions associated with its processing, 75,83,155,195 efforts to trace the diffusion of these effects across the processing hierarchy have produced mixed results. [60][61][62]67,79 For example, Utzerath et al 67 found evidence of RS, ES, and an interaction between expectation and repetition in area LOC.…”