Elsevier

Hearing Research

Volume 258, Issues 1–2, December 2009, Pages 28-36
Hearing Research

Research papers
Multisensory anatomical pathways

https://doi.org/10.1016/j.heares.2009.04.017Get rights and content

Abstract

In order to interact with the multisensory world that surrounds us, we must integrate various sources of sensory information (vision, hearing, touch…). A fundamental question is thus how the brain integrates the separate elements of an object defined by several sensory components to form a unified percept. The superior colliculus was the main model for studying multisensory integration. At the cortical level, until recently, multisensory integration appeared to be a characteristic attributed to high-level association regions. First, we describe recently observed direct cortico-cortical connections between different sensory cortical areas in the non-human primate and discuss the potential role of these connections. Then, we show that the projections between different sensory and motor cortical areas and the thalamus enabled us to highlight the existence of thalamic nuclei that, by their connections, may represent an alternative pathway for information transfer between different sensory and/or motor cortical areas. The thalamus is in position to allow a faster transfer and even an integration of information across modalities. Finally, we discuss the role of these non-specific connections regarding behavioral evidence in the monkey and recent electrophysiological evidence in the primary cortical sensory areas.

Introduction

The cerebral network for multisensory integration was classically viewed as a hierarchically converging system in which the different sensory channels were merging in the polysensory associative areas of the frontal, temporal or parietal lobes. In support of this view was the absence of strong anatomical links between the areas of different modalities at the level of the first stages of sensory processing (see Jones and Powell, 1970). Recent anatomical and electrophysiological studies in non-human primates as well as human functional brain studies led to a reappraisal of this concept (see Ghazanfar and Schroeder, 2006, Driver and Noesselt, 2008 for recent reviews) and highlight that the mechanisms for multisensory interplay are believed to include several levels of brain processing, from the thalamus to the primary sensory areas and higher stages of sensory processing. Such an increase in the diversity of the pathways by which multisensory interactions can occur is probably reflecting an adaptive mechanism by which individual perceptual or sensory-motor situations involve a specific multisensory network. We describe in this review connections in the brain that may represent the support for early multisensory integration, such as cortico-cortical connections and connections between the thalamus and the cortex.

Section snippets

Heteromodal connections: connections between different sensory areas

The convergence of different sensory information channels in polysensory cortical areas is now clearly established and will not be detailed in the present report. Most areas in the parietal, temporal, or frontal regions of primates have connection patterns that relate them to more than one sensory modality. This is particularly the case for the areas buried in the intraparietal sulcus (LIP, VIP) which present anatomical links with cortical areas of different sensory modalities (Lewis and Van

Role of the thalamus

Although mutisensory integration has been shown to take place essentially in the cerebral cortex and the superior colliculus (Stein and Meredith, 1993), one may consider the possibility of complementary contributions taking place at a subcortical level. In this context, given the extensive connections between the neocortex, the superior colliculus and the thalamus, different authors have proposed that subcortical structures integrate the senses even before the neocortex (Ghazanfar and

Role of non-specific connections?

Previous psychophysical studies in humans have shown that a multisensory stimulation can give rise to a percept that differs from that derived from a single modality (e.g. Stein and Meredith, 1993). Such multisensory processing can affect a range of different behavioral parameters, such as reaction times (Welch and Warren, 1986, Raab, 1962), stimulus detection rate (Grant and Seitz, 2000), accuracy of stimulus identification (Giard and Peronnet, 1999) as well as learning effects on stimulus

Conclusion

Thus, recent anatomical and electrophysiological approaches provide evidence that multisensory interactions can be observed at early stages of sensory processing. However, the complexity of the connectivity network involved in multisensory interplay, that includes cortical and thalamo-cortical pathways as well as the diversity of interactions observed across the thalamus, the cortical sensory or associative areas, favor a distributed system that is probably adapted to specific behavioral

Acknowledgements

We thank M. Murray for correcting and comments on the text. Grants supports: the CNRS ATIP program (to P.B.), the Swiss National Science Foundation, grants 31-61857.00 (to E.M.R.) and 310000-110005 (to E.M.R.), the Swiss National Science Foundation Center of Competence in Research (NCCR) on « Neural plasticity and Repair » (to E.M.R.).

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