The ability to use cues from multiple senses in concert is a fundamental aspect of brain function. It maximizes the brain’s use of the information available to it at any given moment and enhances the physiological salience of external events. Because each sense conveys a unique perspective of the external world, synthesizing information across senses affords computational benefits that cannot otherwise be achieved. Multisensory integration not only has substantial survival value but can also create unique experiences that emerge when signals from different sensory channels are bound together. However, neurons in a newborn’s brain are not capable of multisensory integration, and studies in the midbrain have shown that the development of this process is not predetermined. Rather, its emergence and maturation critically depend on cross-modal experiences that alter the underlying neural circuit in such a way that optimizes multisensory integrative capabilities for the environment in which the animal will function.

Single neuron studies provide one foundation for understanding many facets of multisensory integration. These studies have used a variety of criteria for identifying and quantifying multisensory integration. While a number of techniques have been used, there lacks an explicit discussion of the assumptions, criteria, and analytical methods traditionally used to define the principles of multisensory integration. This was not problematic when the field was small, but with rapid growth a number of alternative techniques and models have been introduced, each with its own criteria and sets of implicit assumptions to define and characterize what is thought to be the same phenomenon. The potential for misconception prompted this reexamination of traditional approaches in order to clarify their underlying assumptions and analytic techniques. The objective is to review the traditional quantitative methods advanced in the study of single-neuron physiology in order to appreciate the process of multisensory integration and its impact.

Individual superior colliculus (SC) neurons integrate information from multiple sensory sources to enhance their physiological response. The response of an SC neuron to a cross-modal stimulus combination can not only exceed the best component unisensory response but can also exceed their arithmetic sum (i.e., superadditivity). The present experiments were designed to investigate the temporal profile of multisensory integration in this model system. We found that cross-modal stimuli frequently shortened physiological response latencies (mean shift, 6.2 ms) and that response enhancement was greatest in the initial phase of the response (the phenomenon of initial response enhancement). The vast majority of the responses studied evidenced superadditive computations, most often at the beginning of the multisensory response.

The multisensory integration capabilities of superior colliculus neurons emerge gradually during early postnatal life as a consequence of experience with cross-modal stimuli. Without such experience neurons become responsive to multiple sensory modalities but are unable to integrate their inputs. The present study demonstrates that neurons retain sensitivity to cross-modal experience well past the normal developmental period for acquiring multisensory integration capabilities. Experience surprisingly late in life was found to rapidly initiate the development of multisensory integration, even more rapidly than expected based on its normal developmental time course. Furthermore, the requisite experience was acquired by the anesthetized brain and in the absence of any of the stimulus-response contingencies generally associated with learning. The key experiential factor was repeated exposure to the relevant stimuli, and this required that the multiple receptive fields of a multisensory neuron encompassed the cross-modal exposure site. Simple exposure to the individual components of a cross-modal stimulus was ineffective in this regard. Furthermore, once a neuron acquired multisensory integration capabilities at the exposure site, it generalized this experience to other locations, albeit with lowered effectiveness. These observations suggest that the prolonged period during which multisensory integration normally appears is due to developmental factors in neural circuitry in addition to those required for incorporating the statistics of cross-modal events; that neurons learn a multisensory principle based on the specifics of experience and can then apply it to other stimulus conditions; and that the incorporation of this multisensory information does not depend on an alert brain.

Multisensory Integration describes a process by which information from different sensory systems is combined to influence perception, decisions, and overt behavior. Despite a widespread appreciation of its utility in the adult, its developmental antecedents have received relatively little attention. Here we review what is known about the development of multisensory integration, with a focus on the circuitry and experiential antecedents of its development in the model system of the multisensory (i.e., deep) layers of the superior colliculus. Of particular interest here are two sets of experimental observations: 1) cortical influences appear essential for multisensory integration in the SC, and 2) postnatal experience guides its maturation. The current belief is that the experience normally gained during early life is instantiated in the cortico-SC projection, and that this is the primary route by which ecological pressures adapt SC multisensory integration to the particular environment in which it will be used.Multisensory Integration describes a process by which information from different sensory systems is combined to influence perception, decisions, and overt behavior. All brains engage this strategy at multiple levels of the neuraxis , and its impact on cognition and behavior has been repeatedly demonstrated. Multisensory integration has been shown to enhance and speed the detection, localization, and reaction to biologically significant events (Corneil and Munoz, 1996;Frens and Van Opstal, 1995;Hughes et al., 1994;Stein et al., 1989;Marks, 2004;Newell, 2004;Woods and Recanzone, 2004a;Shams et al., 2004;Sathian and Prather, 2004;. It is also a potent asset in signal disambiguation, including signals involving human speech and animal communication (Senkowski et al., 2007;Busse et al., 2005;Woldorff et al., 2004;Sathian, 2005;Grant et al., 2000;Sathian, 2000;Lakatos et al., 2007;Recanzone, 1998;King and Palmer, 1985;Schroeder and Foxe, 2004;Recanzone, 1998;Ghazanfar and Schroeder, 2006;Sathian and Prather, 2004;Weisser et al., 2005;Zangaladze et al., 1999;Liotti et al., 1998;Talsma et al., 2006a;Talsma et al., 2006b;Corneil and Munoz, 1996;Frens and Van Opstal, 1995;Hughes et al., 1994;Stein et al., 1989;Marks, 2004;Newell, 2004;Woods and Recanzone, 2004b;Shams et al., 2004;Wallace et al., 1996;Sumby and Pollack, 1954;Massaro, 2004;Ghazanfar et al., 2005;Partan, 2004;Bernstein et al., 2004;Sugihara et al., 2006). The impact of this evolutionary strategy is difficult to overestimate. Yet, despite the widespread and enthusiastic appreciation of its utility in the adult (see Calvert and Lewis, 2004;Spence and Driver, 2004;Ghazanfar and Schroeder, 2006), far less attention has been devoted to examining the Correspondence to: Barry E. Stein, Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Medical Center Blvd., Winston-Salem, NC 27157-1010, Phone: 336-716-4368, Fax: 336-716-4534, Email: bestein@wfubmc.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript ...