The role of motor and environmental visual rhythms in structuring auditory cortical excitability

Abstract

One of the ways we perceive our external world is through the process of active sensing in which biological sensors (e.g. fingers and eyes) sample the environment utilizing mostly rhythmic motor routines. Previous studies indicate that these motor sampling patterns modulate neuronal excitability in sensory brain regions by entraining brain rhythms, a process termed motor-initiated entrainment. Additionally, rhythms of the external environment, that are independent of internal motor commands, are also capable of entraining rhythmic brain activity. The goal of our study was twofold. First, we aimed to investigate the properties of motor-initiated entrainment in the auditory system using the most prominent motor sampling pattern in primates, eye movements. Second, we wanted to determine whether/how motor-initiated entrainment by eye movements interacts with visual environmental entrainment. By examining laminar profiles of neuronal ensemble activity in the primary auditory cortex of non-human primates, we found that while motor-initiated entrainment has a suppressive, visual environmental entrainment has an enhancive effect. We also found that the two processes are temporally coupled during free viewing, and their temporal relationship ensures that their effect on neuronal ensemble excitability is complementary rather than interfering. Taken together, our results provide strong evidence that motor and sensory systems continuously interact in orchestrating the brain's rhythmic context for the optimal sampling of our multisensory environment. 3

Saccade-related modulation of oscillatory activity in primary auditory cortex

“…1B). The slight decrease in MUA around saccade onset was similar to the saccade-related modulation of excitability in A1 previously reported by O’Connell and colleagues (2020). There is an influx of visual information that occurs near saccade offset/fixation, which occurs in dimly lit or dark environments.…”

“…Saccade-related supramodal modulation suggests that the motor system could lead to coherence of activity across multiple sensory systems and influence sensory processing on a large scale. In addition to the current results showing that saccades can reset the phase of ongoing oscillations in A1, saccades have also been shown to modulate excitability in A1 (O'Connell et al, 2020). Highlighting the fact saccadic modulation of A1 oscillatory activity -27 that these kinds of motor signals can impact sensory processing at the very earliest stages, saccadic eye movements have been shown to lead to oscillatory-type movement of the eardrum even when no auditory stimuli are presented (Gruters et al, 2018).…”

“…Recently, saccade-related eardrum motion has been observed in the absence of auditory stimuli and this motion appeared to have oscillatory characteristics (Gruters et al, 2018). Additionally, saccade-related entrainment and modulation of excitability has been shown to occur in A1 of NHPs (O’Connell et al, 2020). Although perceptual saccadic suppression of auditory stimuli presented during saccades has not yet been demonstrated (Harris and Lieberman, 1996), saccades have been shown to influence the perception of auditory stimulus localization (Krüger et al, 2016).…”

“…Building on our previous results (O’Connell et al, 2020), the main goal of the current study was to further examine saccade-related entrainment in A1. Linear array multielectrodes were used to observe neuroelectric activity across all layers of A1 in macaque monkeys, while eye movements were monitored as they sat passively in a dark or dimly lit room.…”

Saccadic modulation of neural excitability in auditory areas of the neocortex

“…Intriguingly, several studies suggest that the influence of saccades on neural activity extends beyond the visual system. Sensitivity to static eye position has been noted in both subcortical and cortical auditory pathway structures 23,24 and dynamic saccadic modulation has been observed in the non-visual nuclei of the anterior thalamus 25 as well as in the auditory cortex 26 . Notably, in both monkeys and humans, the eardrum moves in synchrony with saccades 27 .…”