Auditory input enhances somatosensory encoding and tactile goal-directed behavior

Abstract

The capacity of the brain to encode multiple types of sensory input is key to survival. Yet, how neurons integrate information from multiple sensory pathways and to what extent this influences behavior is largely unknown. Using two-photon Ca2+ imaging, optogenetics and electrophysiology in vivo and in vitro, we report the influence of auditory input on sensory encoding in the somatosensory cortex and show its impact on goal-directed behavior. Monosynaptic input from the auditory cortex enhanced dendritic and somatic encoding of tactile stimulation in layer 2/3 (L2/3), but not layer 5 (L5), pyramidal neurons in forepaw somatosensory cortex (S1). During a tactile-based goal-directed task, auditory input increased dendritic activity and reduced reaction time, which was abolished by photoinhibition of auditory cortex projections to forepaw S1. Taken together, these results indicate that dendrites of L2/3 pyramidal neurons encode multisensory information, leading to enhanced neuronal output and reduced response latency during goal-directed behavior.

Integration of somatosensory and motor-related information in the auditory system

“…Simultaneous audio-tactile stimulation can improve reaction times ( Sperdin et al, 2009 ; Godenzini et al, 2021 ) and stimulus detection ( Schürmann et al, 2004 ; Gillmeister and Eimer, 2007 ; Ro et al, 2009 ), and increase perceived loudness ( Gillmeister and Eimer, 2007 ; Yarrow et al, 2008 ). These interactions have been shown to occur in a frequency-dependent manner ( Ro et al, 2009 ; Tajadura-Jiménez et al, 2009 ; Wilson et al, 2010a , b ), with the largest perceptual improvements reported when the frequencies of the auditory and vibrotactile stimuli are closely matched ( Ro et al, 2009 ; Wilson et al, 2010b ).…”

“…In addition to the higher-level cortical association areas implicated in the representation of peripersonal space, multisensory signals have been found to converge throughout the cortex, including in auditory, somatosensory and visual early cortical areas (reviewed in Ghazanfar and Schroeder, 2006 ; Meijer et al, 2019 ). Thus, responses to auditory stimulation in somatosensory cortical areas have been reported in both human fMRI ( Liang et al, 2013 ; Pérez-Bellido et al, 2018 ; Rahman et al, 2020 ) and magnetoencephalography studies ( Lütkenhöner et al, 2002 ), as well as in single-neuron measurements in monkeys ( Zhou and Fuster, 2004 ) and mice ( Carvell and Simons, 1986 ; Zhang et al, 2020 ; Godenzini et al, 2021 ). More attention has been paid, however, to the way that other sensory modalities affect activity in the auditory cortex, with somatosensory influences demonstrated using a range of methods and in several different species ( Foxe et al, 2002 ; Fu et al, 2003 ; Brosch et al, 2005 ; Kayser et al, 2005 ; Schürmann et al, 2006 ; Lakatos et al, 2007 ; Lemus et al, 2010 ; Iurilli et al, 2012 ; Nordmark et al, 2012 ; Hoefer et al, 2013 ; Rao et al, 2014 ; Lohse et al, 2021 ).…”

“…Convergence of inputs from different modalities in early cortical areas could arise from direct connections between those areas, feedback from higher-level associations areas, or be inherited from subcortical inputs ( Driver and Noesselt, 2008 ; Cappe et al, 2012 ). In the case of audio-tactile interactions, connections between somatosensory cortex and auditory cortex have been described in several species ( Cappe and Barone, 2005 ; Budinger et al, 2006 ; Hackett et al, 2007a ; Ro et al, 2013 ; Meredith and Allman, 2015 ; Godenzini et al, 2021 ). This is illustrated in Figure 6 for studies carried out in humans ( Figure 6A ) and in gerbils ( Figure 6B ).…”

“…It remains to be determined whether connections from somatosensory cortex to auditory cortical areas, including A1, are causally involved in the multisensory interactions observed physiologically. However, Godenzini et al (2021) recently reported that photoinhibition of the auditory cortical projection to the forepaw region of the primary somatosensory cortex (S1) eliminated the sound-induced reduction in reaction time on a tactile detection task. This finding, along with other studies of cortical circuitry (reviewed by Meijer et al, 2019 ), indicates that corticocortical connections are likely to play an important role in mediating multisensory influences on perception and behavior.…”

“…Adapted from Lohse et al (2021). Godenzini et al, 2021). This is illustrated in Figure 6 for studies carried out in humans (Figure 6A) and in gerbils (Figure 6B).…”