A system of multimodal areas in the primate brain.

The primate cerebral cortex has traditionally been divided into separate territories for vision, touch, audition and movement. These functions are known to overlap in many parts of cortex, but until recently the regions of overlap were not well studied. In this issue of NeuronBremmer et al. 2000xBremmer, F., Schlack, A., Shah, N.J., Zafiris, O., Kubischik, M., Hoffmann, K.-P., Zilles, K., and Fink, G.R. Neuron. 2000; 29: 287–296Abstract | Full Text | Full Text PDF | Scopus (485)See all ReferencesBremmer et al. 2000 report a major advance in understanding at least one set of areas in the human brain in which the senses are integrated. This finding joins a growing set of work in monkeys and humans on the integration of the senses with each other and with the control of movement.Vision, touch, and audition converge in many areas of the monkey brain, including the deep layers of the superior colliculus, the superior temporal polysensory area, the putamen, the intraparietal sulcus, and parts of premotor cortex (Graziano and Gross 1996xSee all ReferencesGraziano and Gross 1996). Multimodal responses can also be induced in a variety of brain areas with appropriate training. Tell a person to imagine a picture of a cat, and visual cortex becomes active; in this case, an entrained auditory signal activates a part of cortex that is usually only visual (Goldenberg et al. 1989xGoldenberg, G., Podreka, I., Steiner, M., Willmes, K., Suess, E., and Deecke, L. Neuropsychologia. 1989; 27: 641–664Crossref | PubMed | Scopus (118)See all ReferencesGoldenberg et al. 1989). Train a monkey to associate a felt object or a sound with a picture, and visual cortical areas respond to these nonvisual stimuli (Heanny et al., 1988; Colombo and Gross 1994xColombo, M. and Gross, C.G. Behav. Neurosci. 1994; 108: 443–455Crossref | PubMed | Scopus (81)See all ReferencesColombo and Gross 1994). In other words, perhaps as a function of mental imagery, the neurons can respond to a range of sensory stimuli.Among this catalog of multimodal brain areas, one interconnected set of areas stands out for its distinctive response properties. These areas are shown in Fig. 1Fig. 1 in a side view of the monkey brain. Neurons in these areas respond to the sight, sound, and feel of objects moving in the space near the body, usually within reaching distance (Graziano and Gross 1998xSee all ReferencesGraziano and Gross 1998). These responses do not depend on training the monkey on a task and are robust even in anesthetized monkeys. Most of these multimodal neurons are directionally selective. They may respond, for example, to a tactile stimulus swept across the skin in one direction, but not in the opposite direction. The same neurons will usually have a matching directional preference for visual stimuli moving in the space near the tactile receptive field. Some neurons prefer visual stimuli moving toward or away from the body.Fig. 1Side View of a Macaque Monkey Brain Showing the Location of Four Interconnected Multimodal AreasVIP: ventral intraparietal area.View Large Image | View Hi-Res Image | Download PowerPoint SlideThese multimodal response have been studied most thoroughly in monkey premotor cortex (9xRizzolatti, G., Scandolara, C., Matelli, M., and Gentilucci, M. Beh Brain Res. 1981; 2: 147–163Crossref | PubMed | Scopus (349)See all References, 7xGraziano, M.S.A., Hu, X.T., and Gross, C.G. J. Neurophys. 1997; 77: 2268–2292PubMedSee all References). Though sensory responses can be found throughout all of premotor cortex, especially in trained monkeys, this particular type of multimodal response to nearby objects is found only in a few clusters usually just posterior to the bend in the arcuate sulcus. Fig. 2Fig. 2 shows the response properties of two bimodal, visual-tactile neurons studied in premotor cortex. In each case, the neuron responded when the monkey saw or felt an object near a particular part of the body. Other neurons in premotor cortex are trimodal, responding to tactile, visual, and auditory stimuli. Remarkably, these trimodal neurons are able to distinguish the distance to the sound source; they respond best to nearby sounds regardless of the intensity of the stimulus (Graziano et al. 1999xGraziano, M.S.A., Reiss, L.A.J., and Gross, C.G. Nature. 1999; 397: 428–430Crossref | PubMed | Scopus (170)See all ReferencesGraziano et al. 1999).Fig. 2Two Examples of Bimodal, Visual-Tactile Neurons from Premotor CortexIn both cases, the tactile receptive field (stippled) matched the location of the visual receptive field (outlined).View Large Image | View Hi-Res Image | Download PowerPoint SlideAlmost identical neuronal responses encoding the space near the body have been described in the putamen and also in areas 7b and VIP in the parietal lobe (2xColby, C.L., Duhamel, J.-R., and Goldberg, M.E. J. Neurophysiol. 1993; 69: 902–914PubMedSee all References, 5xSee all References). These brain areas are all monosynaptically interconnected and therefore appear to form a single integrated system. However, even though the sensory properties of these neurons have been extensively characterized, their function is still unknown. One hypothesis is that they detect and localize threatening objects near the body and help to organize a defensive reaction.Does the human brain also contain a set of areas that processes the sight, sound, and feel of objects moving in the space near the body? Bremmer et al. 2000xBremmer, F., Schlack, A., Shah, N.J., Zafiris, O., Kubischik, M., Hoffmann, K.-P., Zilles, K., and Fink, G.R. Neuron. 2000; 29: 287–296Abstract | Full Text | Full Text PDF | Scopus (485)See all ReferencesBremmer et al. 2000 presented visual, tactile, and auditory stimuli to human subjects in an MRI scanner. These three types of stimulation were presented on separate trials. The tactile stimulus was a stream of air blowing across the face. The visual stimulus was a display of moving dots on a screen. The auditory stimulus, presented through headphones, gave the illusion of a sound source travelling in front of the subject's face from one side to the other. As expected, the moving visual stimulus, when compared to a control stimulus that was stationary, activated areas in the occipital, temporal, and parietal lobes that are known to be visually responsive. The tactile stimulus, when compared to a resting control condition, activated primary and secondary somatosensory areas. The auditory stimulus, when compared to a resting control condition, activated primary and secondary auditory areas. Thus, the traditional, separate territories for vision, touch, and audition were engaged.In addition to these expected activations in the primary and secondary sensory areas, other presumably higher-order brain areas were also activated. Several brain areas in particular appeared to be multimodal. They became active whether visual, tactile, or auditory stimuli were presented. One of these multimodal areas was located in the intraparietal sulcus, closely matching the location of the multimodal area VIP in the monkey brain as shown in Fig. 1Fig. 1. A second area was in a restricted part of premotor cortex, closely matching the multimodal region of monkey premotor cortex. A third area was in the upper bank of the lateral fissure. The correspondence to the monkey brain is less clear in this case. Part of monkey area 7b extends into the upper bank of the lateral fissure and therefore perhaps corresponds to this region of activation in the human brain. There are, however, other areas in the monkey lateral fissure that may also be multimodal but that are almost totally unstudied (Robinson and Burton 1980xRobinson, C.J. and Burton, H.J. Comp. Neurol. 1980; 192: 93–108Crossref | PubMedSee all ReferencesRobinson and Burton 1980). Clearly more monkey single-neuron experiments are now needed to explore this relatively unknown territory.In summaryBremmer et al. 2000xBremmer, F., Schlack, A., Shah, N.J., Zafiris, O., Kubischik, M., Hoffmann, K.-P., Zilles, K., and Fink, G.R. Neuron. 2000; 29: 287–296Abstract | Full Text | Full Text PDF | Scopus (485)See all ReferencesBremmer et al. 2000 show that the human brain contains a system of multimodal areas similar to those in the monkey brain. The function of these areas is not yet clear. As in the case of the monkey, perhaps they play a role in detecting nearby threatening objects and coordinating a defensive reaction.