Early multisensory integration of self and source motion in the auditory system

Abstract

Discriminating external from self-produced sensory inputs is a major challenge for brains. In the auditory system, sound localization must account for movements of the head and ears, a computation likely to involve multimodal integration. Principal neurons (PNs) of the dorsal cochlear nucleus (DCN) are known to be spatially selective and to receive multimodal sensory information. We studied the responses of PNs to body rotation with or without sound stimulation, as well as to sound source rotation with stationary body. We demonstrated that PNs are sensitive to head direction, and, in the presence of sound, they differentiate between body and sound source movement. Thus, the output of the DCN provides the brain with enough information to disambiguate the movement of a sound source from an acoustically identical relative movement produced by motion of the animal.dorsal cochlear nucleus | multisensory integration | sound localization A significant amount of sensory information reaching the brain of a moving organism results from the movement itself. Organisms have to disentangle self-generated sensations from the rest of the sensory input to use external sensory information for guiding behavior. To perform this disentanglement, brains integrate information from different sensory modalities and use efference copies of motor commands (1-3). This difficult challenge has been studied in several sensory-motor systems. In the visual system, the organism has to discriminate between movement of the visual scene and movement of the eyes (4, 5). Similarly, in the auditory system, it is necessary to discriminate between an actual motion of a sound source and the relative motion caused by movement of the head or the body (6). Moreover, it has recently been demonstrated that spatial acuity is improved during self-motion in comparison with sound-source motion (7). Here we show that neurons of the dorsal cochlear nucleus (DCN), which are known to be spatially selective (8,9), are affected by vestibular stimulation. We demonstrate that by integrating these two sensory modalities, the output of the DCN already contains enough information to reliably discriminate between self and sound-source motions.The DCN is a dome-like formation located on the dorsal surface of the lower medulla. Its anatomy and physiology have been thoroughly studied both in vivo and in vitro (9, 10). The principal neurons (PNs) of the DCN, the fusiform and giant cells, receive auditory information directly from the auditory nerve (11), as well as indirectly from other neurons in the cochlear nucleus. The DCN has cerebellar-like circuitry (9). A large number of granule cells contribute to a parallel fiber-like system that forms a molecular layer and conveys multimodal sensory information to the molecular layer interneurons as well as the PNs and cartwheel cells (9,(12)(13)(14) (Fig. 1A). Interneurons within the molecular layer, including the cartwheel cells, form inhibitory local networks that terminate on the PNs.Sound localization in mammals is based on binau...

Egocentric and Allocentric Representations in Auditory Cortex

“…Furthermore, coordinate transformations occur elsewhere in the auditory system [36,37] and behavioral movements can influence auditory subcortical and cortical processing [27,28]. Perhaps most importantly, vestibular signals are integrated into auditory processing already at the level of the cochlea nucleus [38] allowing the distinction between self and source motion [22]. Auditoryvestibular integration, together with visual, proprioceptive and motor corollary discharge systems, provides a mechanism through which changes in head direction can partially offset changes in acoustic input during movement to create allocentric representations.…”

“…While it has been largely assumed cortical neurons represent sound location relative to the head, the spatial coordinate frame in which location is encoded remains to be demonstrated. Furthermore, though the acoustic cues to sound localisation are explicitly head-centered, information about head direction necessary to form a world-centered representation is present at early levels of the ascending auditory system [22]. Thus it may be possible for neurons in the auditory system to represent space in an allocentric, world-centered coordinate frame that would preserve sound location across self-generated movement.…”

Re-evaluating Circuit Mechanisms Underlying Pattern Separation

“…However, in the past decade, anatomical (Huang et al, 2013) and physiological evidence (Proville et al, 2014) has accumulated for mixed representations generated through multimodal integration in single granule cells of the cerebellar cortex (Arenz et al, 2008;Chabrol et al, 2015;Ishikawa et al, 2015). Multimodal integration has also been observed in granule cells of the mammalian auditory system (Wigderson et al, 2016) and electrosensory system of weakly electric fish (Sawtell, 2010), which have a ''cerebellar-like'' circuitry (Oertel and Young, 2004;Bell et al, 2008;Kennedy et al, 2014;Singla et al, 2017). Mixed representations in the dentate gyrus are harder to ascertain, because entorhinal cortical neurons already integrate multisensory cues to generate spatial representations (Campbell et al, 2018).…”

Multisensory activation of ventral cochlear nucleus D‐stellate cells modulates dorsal cochlear nucleus principal cell spatial coding

“…To control for possible alterations to fusiform cell firing rates by changing body position (Wigderson et al . ), which may obscure I ‐width calculation, we recorded rate‐level functions for broad‐band noise (BBN) stimulation during each condition (Fig. D ) and found that tilt change did not affect fusiform cell spontaneous or evoked firing rates (two‐way ANOVA, F (17,2) = 0.26, P = 0.77).…”

“…; Koehler & Shore, ; Wigderson et al . ), a second‐order station for coding sound location (May, ; Young & Davis, ). But how multisensory information functionally influences brainstem sound localization processing has not been elucidated.…”