Attenuation of Responses to Self-Generated Sounds in Auditory Cortical Neurons

Abstract

Many of the sounds that we perceive are caused by our own actions, for example when speaking or moving, and must be distinguished from sounds caused by external events. Studies using macroscopic measurements of brain activity in human subjects have consistently shown that responses to self-generated sounds are attenuated in amplitude. However, the underlying manifestation of this phenomenon at the cellular level is not well understood. To address this, we recorded the activity of neurons in the auditory cortex of mice in response to sounds generated by their own behavior. We found that the responses of auditory cortical neurons to these self-generated sounds were consistently attenuated, compared with the same sounds generated independently of the animals' behavior. This effect was observed in both putative pyramidal neurons and in interneurons and was stronger in lower layers of auditory cortex. Downstream of the auditory cortex, we found that responses of hippocampal neurons to self-generated sounds were almost entirely suppressed. Responses to selfgenerated optogenetic stimulation of auditory thalamocortical terminals were also attenuated, suggesting a cortical contribution to this effect. Further analyses revealed that the attenuation of self-generated sounds was not simply due to the nonspecific effects of movement or behavioral state on auditory responsiveness. However, the strength of attenuation depended on the degree to which self-generated sounds were expected to occur, in a cell-type-specific manner. Together, these results reveal the cellular basis underlying attenuated responses to self-generated sounds and suggest that predictive processes contribute to this effect.

Irrelevant Predictions: Distractor Rhythmicity Modulates Neural Encoding in Auditory Cortex

“…One way to interpret the suppression of sensory responses in auditory cortex for rhythmic distractors is within the predictive-coding framework, which posits that evoked response for predictable stimuli are reduced, reflecting a smaller prediction-error (Lange 2009;Bastos et al 2012;van Atteveldt et al 2015;Rummell et al 2016;Sherwell et al 2017;Friston 2019). According to this interpretation, the effects of predictability on sensory encoding of sounds that are to-be-ignored, are qualitatively similar to previously reported effect of for attended sounds (Sherwell et al 2017).…”

How Do Expectations Shape Perception?

“…Overall, stimuli that are expected evoke a reduced neural response. This pattern has been observed when stimuli are validly predicted by a preceding, arbitrarily paired, stimulus [65][66][67][68][69], when stimuli comply with a higher-order pattern such as a shape or scene [33,34], or when stimuli are the predictable result of an animal's own actions [70]. This phenomenon, termed expectation suppression [64,68,71], is present even when lowlevel adaption is controlled for and has been consistently found across modalities such as vision [65][66][67][72][73][74] and audition [68,69,75,76].…”

The function and failure of sensory predictions

“…Moreover, CD signals are not only critical for the discrimination of self‐produced versus externally generated sounds, but they also enable higher level functions such as learning of acoustic behavior, speech, and music across species by suppressing auditory responses to movement‐related stimulation . Auditory cortical neuron attenuation has been observed at the single‐cell and circuit level using optogenetics in mice, providing important tools for our understanding of neural circuit dysfunction in diseases such as schizophrenia …”