Physiological and Anatomical Evidence for Multisensory Interactions in Auditory Cortex

Abstract

Recent studies, conducted almost exclusively in primates, have shown that several cortical areas usually associated with modalityspecific sensory processing are subject to influences from other senses. Here we demonstrate using single-unit recordings and estimates of mutual information that visual stimuli can influence the activity of units in the auditory cortex of anesthetized ferrets. In many cases, these units were also acoustically responsive and frequently transmitted more information in their spike discharge patterns in response to paired visual--auditory stimulation than when either modality was presented by itself. For each stimulus, this information was conveyed by a combination of spike count and spike timing. Even in primary auditory areas (primary auditory cortex [A1] and anterior auditory field [AAF]),~15% of recorded units were found to have nonauditory input. This proportion increased in the higher level fields that lie ventral to A1/AAF and was highest in the anterior ventral field, where nearly 50% of the units were found to be responsive to visual stimuli only and a further quarter to both visual and auditory stimuli. Within each field, the pure-tone response properties of neurons sensitive to visual stimuli did not differ in any systematic way from those of visually unresponsive neurons. Neural tracer injections revealed direct inputs from visual cortex into auditory cortex, indicating a potential source of origin for the visual responses. Primary visual cortex projects sparsely to A1, whereas higher visual areas innervate auditory areas in a field-specific manner. These data indicate that multisensory convergence and integration are features common to all auditory cortical areas but are especially prevalent in higher areas.

Cortico‐cortical connectivity within ferret auditory cortex

“…The anterior bank of the PSSC projects to the superior colliculus (Bajo et al, 2010a), and is likely to be homologous to the anterior ectosylvian sulcal field (fAES) of the cat (Jiang et al, 1996; Manger et al, 2005). In accordance with the suggestion that cat fAES may be specialized for spatial processing (Middlebrooks et al, 1998; Malhotra and Lomber, 2007; Las et al, 2008), it has been shown that inputs to the aPSSC from the visual cortex arise predominantly from area SSY (Bizley et al, 2007a), which is thought to be specialized for visual motion processing (Philipp et al, 2006). Previous studies of the PSSC have not demarcated the anterior and posterior banks.…”

“…Previous tracer studies in ferret revealed that these areas are innervated by the ventral division of the MGB (Pallas et al, 1990), and that multiple areas, predominantly on the PEG, but also on the AEG, receive connections from the MEG (Wallace and Bajwa, 1991; Pallas and Sur, 1993; Gao and Pallas, 1999). Since these studies were completed, we have gained a deeper understanding of the functional organization of the auditory cortex as assessed by responses to both simple (Kowalski et al, 1995; Nelken et al, 2004; Bizley et al, 2005, 2007a) and complex stimuli (Nelken et al, 2008; Bizley et al, 2009, 2013; Atiani et al, 2014), warranting a more comprehensive investigation of the connectivity within the auditory cortex. Our anatomical investigations support the idea that distinct anterior and posterior processing pathways exist and extend our understanding about the organization of the auditory cortex in the ferret, thus providing crucial information to facilitate cross‐species comparisons.…”

“…The anatomical data presented here also support the parcellation of the anterior bank into at least three areas: the ADF, which is not tonotopically organized and receives inputs predominantly from the AAF, PSF, and AVF; the AVF, a multisensory area whose inputs from the EG arise principally from the ADF; and the aPSSC, which is innervated by the PSF, ADF, and AVF. Each of these regions also receives cortical inputs originating outside the EG (Ramsay and Meredith, 2004; Manger et al, 2005; Bizley et al, 2007a). …”

“…Differences in the connectivity patterns between anterior and posterior areas are consistent with the presence of functionally distinct processing streams. Given the specificity with which visual cortical fields innervate the auditory cortex (Bizley et al, 2007a), it seems likely that, as in the monkey (Hackett et al, 1999; Romanski et al, 1999), distinct differences may exist in the projections from the ferret auditory cortex to prefrontal and parietal areas, although this remains to be tested. Finally, the convergence and divergence of connections found throughout the auditory cortex suggest that behaviorally relevant information can be processed in parallel, providing a potential substrate for compensatory plasticity when specific cortical fields are removed or inactivated for prolonged periods.…”

“…These studies have shown that regions on the posterior bank are more strongly connected with the MEG than those on the anterior bank (Pallas and Sur, 1993). Several studies have looked at connections between specific fields located on the ectosylvian gyrus (EG) and other sensory cortices (Ramsay and Meredith, 2004; Manger et al, 2005; Bizley et al, 2007a; Keniston et al, 2009), and at the descending, subcortical connections that originate in the auditory cortex (Bajo et al, 2007, 2010a, b). A comprehensive anatomical investigation of cortico‐cortical connectivity within the EG of this species has not, however, been carried out.…”