Review article
Motor output, neural states and auditory perception

https://doi.org/10.1016/j.neubiorev.2018.10.021Get rights and content

Highlights

  • Interactions between neural states and stimulus attributes affect perception.

  • We outline a mechanism by which motor cortex shifts neural states in auditory cortex.

  • Such shifts are driven by global inhibition exerted during motor cortex engagement.

  • Our mechanism explains behavioral and neural phenomena of sensory modulation.

Abstract

Behavior is a complex product of interactions between sensory influx arising from the environment and the neural state of the organism. Therefore, identical sensory input can elicit different behavioral responses. Research in recent years has demonstrated that perception is modulated when an organism is engaged in active behavior – suggesting that neural activity in motor pathways is one factor governing the neural state of networks engaged in sensory processing. In the current manuscript, we focus on the auditory modality and propose a mechanism by which activity in motor cortex changes the neural state in auditory cortex through global inhibition. In turn, such global inhibition reduces auditory net population activity, sharpens auditory frequency tuning curves, shifts the auditory oscillatory state and increases the signal-to-noise ratio of auditory evoked neural activity. These changes can result in either attenuated or enhanced behavioral responses depending on the environmental context. We base our model on animal and human literature and suggest that these motor-induced shifts in sensory states may explain reported phenomena and apparent discrepancies in the literature of motor-sensory interactions, such as sensory attenuation or sensory enhancement.

Introduction

Biological organisms continuously interact with the environment. Therefore, behaviors and environmental context are intertwined and constantly shape each other. Although our sensory organs are designed to detect physical changes in the external world, many studies in recent years demonstrate that sensory perception is a product of complex interactions between the physical attributes of sensory stimuli and the neural state of the organism. For example, during stimulation from multiple sources, we are able to filter out irrelevant sensory inputs and extract information originating from a single source by modulating our neural state with attentional effort. In the auditory domain, this phenomenon is known as the “cocktail party effect” (Arons, 1992). Other examples in which sensory stimuli interact with neural state come from bistable perception paradigms, such as Rubin’s vase-face illusion (Rubin, 1915) and binocular rivalry (Wheatstone, 1838) in the visual modality. In such paradigms, the physical properties of the stimulus are constant, yet the percept fluctuates over time. It has been shown that subjects’ perceptual reports were dependent on spontaneous fluctuations in the neural state (Hesselmann et al., 2008; Iemi et al., 2017). Similar findings were also reported in the auditory domain, where detection of near-threshold sounds has been shown to depend on neural activity in auditory cortex preceding sound onset (Sadaghiani et al., 2009). Taken to the extreme, sensory stimulation during neural states associated with sleep can go undetected at the behavioral level.

One factor that shapes the neural state of an organism, and consequently modulates sensory processing, is activity of the motor system, for example during voluntary action execution (Händel and Schölvinck, 2017). In the tactile domain, self-applied strokes are perceived less ticklish compared with identical strokes applied by an external source (the well-known phenomenon that we are not able to tickle ourselves; Blakemore et al., 1998, 1999). Additionally, perceived loudness of auditory tones that are the consequence of voluntary actions is modulated compared with physically identical tones generated by someone else (Sato, 2008; Weiss et al., 2011a; Reznik et al., 2015b). Similar perceptual modulations in the visual domain have been reported as well (Dewey and Carr, 2013; Desantis et al., 2014). Behavioral and neural modulation of sensory-evoked responses due to activity in motor cortex has been widely reported both in humans (Horvath, 2015; Hughes et al., 2013) and animals (Poulet and Hedwig, 2007; Crapse and Sommer, 2008a, b; Schneider and Mooney, 2018), and the functional roles ascribed to such motor-induced modulations include preserving the response sensitivity of sensory organs, learning of motor-sensory contingencies and agency attribution (for elaboration on these functional roles see Box 1). Hence, delineating the parameters that govern the mechanism by which motor actions modulate sensory processing is crucial for understanding complex motor-sensory interactions and their relationship to behavior and cognition.

Although there is evidence for motor-induced sensory modulation in the visual (Bennett et al., 2013) and somatosensory (Blakemore et al., 1998) modalities, in the current manuscript we focus on the auditory modality. Our choice stems from the fact that in the auditory domain, experimental paradigms can precisely equate the physical properties of stimuli across active and passive conditions - something that is more difficult in the somatosensory modality. In the case of vision, to the best of our knowledge, there is no detailed description for direct anatomical connections between motor and visual cortices. On the other hand, direct anatomical connections between motor and auditory cortices, allow us to build a physiologically parsimonious model for motor-auditory modulation.

We start by describing the anatomical connectivity between motor and auditory regions in rodents and primates. Next, we review evidence showing that engagement of motor cortex results in a shift of the neural state in auditory cortex and how responsiveness of auditory neurons depends on environmental context. We continue by describing how motor cortex engagement and environmental context interact to shape auditory cortical responses and perception. To support our proposed mechanism with empirical evidence, we review both animal and human literature. We conclude by pointing to open questions and future research directions.

Although within the auditory modality it is appealing to focus on speech and natural vocalization as the most ecologically relevant type of self-generated auditory stimuli, a few limitations arise. A crucial limitation lies in an inherent methodological difficulty to equate the physical properties of active vocalizations and their passive replay. During vocalization, auditory pathways are stimulated through both bone and air conduction (Reinfeldt et al., 2010). Moreover, vocalizations are associated with stretch of the inner ear muscles (“attenuation reflex”) which reduces the amount of auditory input to the central nervous system (Salomon and Starr, 1963; Borg and Zakrisson, 1975; Suga and Jen, 1975; Hennig et al., 1994; Poulet and Hedwig, 2001). Conversely, during passive perception of recorded playback, the sound is perceived only through air conduction and there are no frequency/intensity shifts associated with stretch of the inner ear – making the two types of stimuli inherently different. Therefore, to avoid potential confounds due to mere differences in physical aspects of the stimulus, we deliberately refrain from discussing paradigms involving speech/vocalizations (e.g., Eliades and Wang, 2003, 2008; Chen et al., 2011; Greenlee et al., 2011), and focus on studies in which physical attributes of the stimuli can be controlled across conditions. These studies typically involve pure tones perceived in the presence or absence of motor cortex engagement (e.g., during voluntary movements or neural stimulations).

Section snippets

Anatomical connectivity between the motor and auditory cortices

Although to date, there is no evidence for direct connections between primary motor cortex and primary auditory cortex, functional-anatomical evidence from rodents and primates point to bi-directional connections between secondary motor regions and associative auditory regions.

In mice and rats, reciprocal connections between secondary motor cortex and the auditory cortex and auditory thalamus have been reported (Reep et al., 1984, 1987; Nelson et al., 2013; Schneider et al., 2014). Moreover,

Motor cortex engagement changes the neural state in auditory cortex

As mentioned above, neurons in mice secondary motor cortex make direct (i.e., monosynaptic) excitatory connections with auditory pyramidal cells and auditory inhibitory interneurons (Nelson et al., 2013; Schneider et al., 2014). The inhibitory interneurons in turn make local connections with auditory pyramidal cells (see Figs. 1 and 2 for schematic representation of motor-auditory circuitry during motor engagement). Therefore, activity in motor regions exerts direct excitation and indirect

Responsiveness of auditory neurons depends on environmental context

One characteristic of the immediate sensory environment is its saliency. At one end are salient environmental contexts in which bottom-up sensory stimulation is well above threshold, easily detectible or can even induce over-stimulation of sensory pathways. At the other end are faint environmental contexts in which sensory inputs are at the organisms’ threshold of detection.

Auditory stimulation results in afferent input to auditory cortex and evoked responses in auditory neurons. Importantly,

Motor cortex engagement and environmental context shape responsiveness of auditory cortex and perception

Motor-induced inhibition results in change in auditory neural state irrespective of environmental context. However, since different environmental contexts are associated with tasks that emphasize different aspects of the neural representation of auditory stimuli, the consequences of motor-induced inhibition may change across environmental contexts. For example, perception of sound loudness (usually performed in salient environmental contexts) may be governed by the amount of responding neurons,

Discussion and open questions

We outline a new perspective on a behavioral and neurophysiological phenomenon of sensory modulation and propose a plausible neurophysiologic model that can reconcile apparent discrepancies in the literature. The reviewed body of literature suggests that motor actions result in (1) reduced auditory net population activity, (2) narrowing of auditory frequency tuning curves, (3) increase in auditory-evoked SNR and (4) shift of the oscillatory activity from synchronized to desynchronized sate.

Acknowledgements

Authors declare no conflict of interest. R.M. was supported by the I-CORE Program of the Planning and Budgeting Committee, and Israel Science Foundation Grant 51/11, Israel Science Foundation Grants 1771/13 and 2043/13. We thank lab members and two anonymous reviewers for fruitful and valuable comments on this manuscript.

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