Visual Modulation of Neurons in Auditory Cortex

Abstract

Our brain integrates the information provided by the different sensory modalities into a coherent percept, and recent studies suggest that this process is not restricted to higher association areas. Here we evaluate the hypothesis that auditory cortical fields are involved in cross-modal processing by probing individual neurons for audiovisual interactions. We find that visual stimuli modulate auditory processing both at the level of field potentials and single-unit activity and already in primary and secondary auditory fields. These interactions strongly depend on a stimulus' efficacy in driving the neurons but occur independently of stimulus category and for naturalistic as well as artificial stimuli. In addition, interactions are sensitive to the relative timing of audiovisual stimuli and are strongest when visual stimuli lead by 20-80 msec. Exploring the underlying mechanisms, we find that enhancement correlates with the resetting of slow (approximately 10 Hz) oscillations to a phase angle of optimal excitability. These results demonstrate that visual stimuli can modulate the firing of neurons in auditory cortex in a manner that depends on stimulus efficacy and timing. These neurons thus meet the criteria for sensory integration and provide the auditory modality with multisensory contextual information about co-occurring environmental events.

Multisensory anatomical pathways

“…In the non-human primate (see also other chapters in this issue), several electrophysiological experiments have similarly revealed audio-visual interactions in the auditory cortex (Ghazanfar et al, 2005;Bizley et al, 2007;Bizley and King, 2008;Cappe et al, 2007b;Kayser et al, 2008) down to the level of A1 (Kayser et al, 2008). These recent results were highly complementary to the pioneer works of Schroeder's laboratory that have revealed the multimodal feature of the monkey auditory belt where both visual and somatosensory responses can be evoked (Schroeder et al, 2001;Schroeder and Foxe, 2002;Fu et al, 2003).…”

“…Although somewhat surprising, there is evidence for the existence of multisensory neurons in areas traditionally considered as unisensory, such as the visual cortex (between areas 17 and 18a) in the rat (Barth et al, 1995) and in the auditory cortex of the monkey (Watanabe and Iwai, 1991;Schroeder et al, 2001;Cappe et al, 2007b;Kayser et al, 2008) and of the ferret (Bizley et al, 2007;Bizley and King, 2008). In addition, previous studies have shown the existence of scattered projections of the auditory cortex towards the visual area 18 in the rat and the cat (Miller and Vogt, 1984;Innocenti et al, 1988).…”

“…The notion that multisensory integration is restricted to higherorder areas has recently been challenged by human and animal studies that have revealed that crossmodal interactions can occur in unisensory areas at very low levels of cortical processing (Buchel et al, 1998;Calvert et al, 1999Calvert et al, , 2001Macaluso et al, 2000;Schroeder et al, 2001;Amedi et al, 2002;Ghazanfar et al, 2005;Kriegstein et al, 2005;Miller and D'Esposito, 2005;Watkins et al, 2006;Martuzzi et al, 2007;Kayser et al, 2007Kayser et al, , 2008Romei et al, 2007Romei et al, , 2008Wang et al, 2008) and more importantly at very short latencies (Giard and Peronnet, 1999;Foxe et al, 2000;Molholm et al, 2002;Murray et al, 2005;Senkowski et al, 2007;Sperdin et al, 2009). Such a fast timing of multisensory interactions rule out an origin in the multisensory areas mediated through backward projections, and instead favor direct heteromodal connections.…”

Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey

“…In marmosets, retrograde tracers in A1 also did not produce labeled cells in early visual areas (Cappe and Barone 2005), but the ferret does have a projection from V1 to A1 (Bizley et al 2007). At least some visual responses have been identified in A1 (Kayser et al 2007(Kayser et al , 2008, but these could arise from other sources besides early visual cortex, for example, from thalamic nuclei or multisensory association areas (Musacchia and Schroeder 2009;Smiley and Falchier 2009). …”

“…Area Tpt was not differentiated in that study but was included as part of CPB. Electrode recordings also showed visual responses across these areas in macaque monkeys, but these did not clearly demonstrate a stronger response in lateral compared with medial areas (Kayser et al 2008). In humans, fMRI studies have not always differentiated between auditory areas, but at least some showed more robust visual activation in caudal areas (e.g., van Atteveldt et al 2004;Lehmann et al 2006;Antal et al 2008).…”