Sensorimotor integration in the auditory dorsal stream

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Project Summary/Abstract Two cortical pathways originate from early core and belt areas of auditory cortex: a ventral pathway subserving identification of sounds, and a dorsal pathway that was originally defined – similar to the visual system – as a processing stream for space and motion. It has been proposed that the auditory dorsal pathway should be reframed in a wider sense as a processing stream for sensorimotor integration and control (Rauschecker, 2011). This broader function explicitly includes spatial processing but also extends to the processing of auditory-motor sequences, including spoken speech and musical melodies in humans. In this long-term project, we will test the expanded model of the auditory dorsal stream by training rhesus monkeys to produce sound sequences on a new behavioral apparatus (“monkey piano”) developed in our laboratory (Archakov et al., 2020). By pressing a lever, the monkey produces a tone of a specific pitch; by pressing several levers in succession, the monkey produces a melody. After an animal has learned to reliably play the same sequence, auditory-responsive brain regions are identified through whole-brain functional magnetic resonance imaging (fMRI) while the animal is alert and listens to the learned self-produced sequence. Control stimuli include melodies the monkey has been passively exposed to, and novel melodies that the monkey has never heard before. Results from the previous funding cycle show that listening to the self-produced melody activates not only auditory areas but also motor regions of the brain, thus demonstrating the existence of internal models linking perception and action. The locations of activated regions will now guide electrophysiological recording with linear microelectrode arrays (LMAs). We will record neuronal responses in auditory and motor regions of cortex to passive listening of the sound sequences and compare them to neuronal activity obtained when the monkey actively produces the sequence with and without sound. Finally, we will add video of a monkey playing the sound sequence on the monkey piano and study multisensory interactions along the dorsal stream using fMRI and LMAs. In particular, responses in caudal auditory belt and parabelt will be compared with those in premotor cortex and posterior parietal cortex in simultaneous recordings. Our studies, using alert monkeys trained in a behavioral task, will contribute to the understanding of unified principles of perception and cognition across sensory systems and their interactions with the motor system in the form of internal models. Investigating the auditory dorsal stream in a nonhuman primate will provide essential information on the origin of human communication, including speech and music. Our studies are relevant for higher–level processing disorders of speech and its production, such as apraxia of speech, non-fluent aphasia, and specific language disorders that involve inadequate coordination between sensory and motor systems. The results will also improve our understanding of sensorimotor disorders, such as ataxia, which may be caused by stroke or neurodegenerative disease, thus leading to better therapies and rehabilitation strategies.