Multisensory connections of monkey auditory cerebral cortex

Abstract

Functional studies have demonstrated multisensory responses in auditory cortex, even in the primary and early auditory association areas. The features of somatosensory and visual responses in auditory cortex suggest that they are involved in multiple processes including spatial, temporal and object-related perception. Tract tracing studies in monkeys have demonstrated several potential sources of somatosensory and visual inputs to auditory cortex. These include potential somatosensory inputs from the retroinsular (RI) and granular insula (Ig) cortical areas, and from the thalamic posterior (PO) nucleus. Potential sources of visual responses include peripheral field representations of areas V2 and prostriata, as well as the superior temporal polysensory area (STP) in the superior temporal sulcus, and the magnocellular medial geniculate thalamic nucleus (MGm). Besides these sources, there are several other thalamic, limbic and cortical association structures that have multisensory responses and may contribute cross-modal inputs to auditory cortex. These connections demonstrated by tract tracing provide a list of potential inputs, but in most cases their significance has not been confirmed by functional experiments. It is possible that the somatosensory and visual modulation of auditory cortex are each mediated by multiple extrinsic sources.

Figure 1

Schematic summaries of the possible sources of non-auditory sensory inputs to auditory cortex are presented. In these schematics, area Tpt is included with the auditory areas, because it has multisensory connections very similar to those of the adjacent caudal auditory areas. Typically, Tpt is not considered an auditory area, but rather an “auditory-related area” (Hackett and Kaas, 2004). The inset at the upper right shows a schematic summary of auditory areas on the ventral bank of the lateral sulcus (Hackett and Kaas, 2004). In monkeys, there are at least 2 core areas (A1 and R, in blue color), surrounded by several belt areas (yellow color), and flanked laterally be parabelt areas and caudally by area Tpt. Additional core and belt areas may lie rostral to R, but these are still poorly defined. In the following schematics, the belt areas surrounding A1 are treated as a single area. Even though the belt connections were demonstrated in areas CM and CL, these connections are assumed to be present as well in MM and ML. A. A summary of somatosensory cortex to auditory cortex connections (red arrows) is shown on a schematic of the opened lateral sulcus. Arrows with dashed lines show connections that are less certain. In both macaques and marmosets, the caudal belt and parabelt, as well as area Tpt, receive inputs at least from Ri and Ig. There is some evidence that these connections are also sparsely present in A1, and there is some evidence that S2 also projects to auditory areas. Similar somatosensory inputs to rostral areas were generally not observed, with the exception of one injection in somatosensory area PV that showed a rostral auditory connection (Disbrow et al., 2003). B. Purple arrows summarize the connections of auditory cortex with areas of early visual processing. Visual inputs to caudal auditory belt, parabelt and Tpt originated in areas V2 and prostriata. Projections from these same auditory areas, and possibly also A1, were found in V2, prostriata, and area V1. Nearly all connections were with the peripheral field representations in visual cortex. C. Black arrows show the connections of several nuclei of the caudal thalamus that project to auditory cortex and may be sources of cross-modal input. All of these multisensory nuclei project to the caudal auditory areas, but the rostral areas receive significant inputs only from MGm, and more sparsely from the medial pulvinar (MP) and the SG. D. Black arrows show inputs from cortical and limbic association areas that might provide multisensory input to auditory cortex. These include areas 23 and 31 located along the caudal cingulate gyrus, area 7a on the inferior parietal cortex, area STP in the superior temporal sulcus, several areas on the lateral surface of the prefrontal cortex, and the claustrum.