Parallel processing in the nervous system: evidence from sensory maps.

Perhaps the clearest organizing principle in sensory systems is the existence of maps, in which there is an orderly and systematic layout of the stimulus space on a two-dimensional array of neurons. Usually, the layout of the stimulus on the receptor sheet is reproduced so that neurons that innervate adjacent sites on the receptor sheet project to adjacent sites in the central map. Thus, in the visual system there are retinotopic maps in which layout of the visual field on the retina is reproduced across a sheet of neurons in the thalamus or cortex. Somatotopic maps of the body surface in the touch system and frequency maps in the auditory system are similar examples. In the olfactory system, the form of the representation is different in that projections from the olfactory epithelium to the first central olfactory nucleus, the olfactory bulb, are sorted according to olfactory receptor molecules (1) and not position on the olfactory epithelium, but the basic principle of sensory mapping seems to be the same. In most systems, there are multiple repetitions of the map at both subcortical and cortical levels. Because all or most of the receptor sheet is contained in each map repetition, each separate representation is a unit in a system of serialyparallel channels making up the overall system. This organization suggests the hypothesis that each map is performing a different type of analysis on the sensory information from the receptors; perception ultimately involves integration of the information from these separate representations. Much recent effort in sensory neurophysiology has gone into trying to define the types of processing done in each map unit and the interactions among units. For example, the visual cortex consists of a complex series of interconnected units of this type (2) that differ in their responsiveness to color, motion, and other aspects of the visual stimulus. It has been suggested that this array of separate representations is organized into two pathways, the first important for motion and spatial relationships between objects and the second important for color, form, and object identification (3). However, the complexity of this system, and of other cortical systems, has made it difficult to assign particular perceptual or behavioral functions to individual maps. The paper by Metzner and Juranek (4) considers sensory maps in the brainstem electrosensory system of weakly electric fish and shows a clear example of a direct relationship between sensory maps and particular behaviors. Parallel sensory maps have been defined in the brainstem in most sensory systems. For example, the mammalian cochlear nucleus contains at least six different principal-cell systems that project in parallel onto higher-order auditory nuclei (5) (Fig. 1). These systems differ dramatically in their morphology, their synaptic relationships to incoming auditory nerve fibers, their postsynaptic integration properties, the degree of interneuronal processing involved, and the targets of their axons. The cochlear nucleus serves below as a comparison with the primary electrosensory nucleus analyzed by Metzner and Juranek. Weakly electric fish have an electric organ that produces an electric field in their vicinity. They are provided with an extensive electrosensory system containing two kinds of receptor cells, tuberous and ampullary, scattered along their outer surface from head to tail. By sensing changes in their own electric fields, the fish can gain information about nearby objects in the water (6). The axons innervating electroreceptors end in the electrosensory lateral line lobe (ELL) in the brainstem (7). The ELL actually contains four complete somatotopic maps of the electroreceptors on the body surface. Axons from the ampullary electroreceptors form one of the maps, and axons from the tuberous receptors form the other three (8); neurons in the three maps related to the tuberous receptors are sensitive to the electric organ discharge and are the subject of this paper. Understanding the functional roles of the separate maps depends on three kinds of evidence. First, there is anatomical evidence. Once the connections, especially the output connections, of a map are known, it may be possible to infer the map’s function from known functions of the neurons that receive their inputs from the map. In the cochlear nucleus, for example, the bushy-cell subsystems (spherical and globular bushy cells in Fig. 1) project exclusively to the principal nuclei of the superior olivary complex (Fig. 1, MSO, LSO, and MnTB). The superior olive is the initial site of comparison of sound in the two ears; this comparison underlies the computation of sound source location based on interaural differences in the arrival time and loudness of a sound (9). These differences are produced by the acoustics of the head and vary in amplitude with the (mainly azimuthal) position of a sound source with respect to the head; thus, they convey information about the location of the source. Because cochlear-nucleus bushy cells project exclusively to the superior olive and are the only inputs to the cells analyzing interaural differences, the bushy-cell maps must be part of the sound localization system. In the case of the ELL, the parallel maps are essentially identical anatomically, do not share interconnections, and project axons to the same structures (10). Although there are some differences in the details of these projection patterns between maps, they do not appear to provide information about function. A second source of evidence comes from the physiological properties of the neurons themselves. By analyzing the response properties of the neurons that make up a map, it may be possible to demonstrate that the neurons are encoding certain aspects of the sensory signal and not others, which may suggest a role for those neurons in the overall sensory analysis. In the example of the bushy cells, their synaptic and membrane physiology is specialized to preserve the timing of actions potentials from their auditory nerve inputs with a precision that is sufficient to support interaural time sensitivity at frequencies up to several kilohertz (5); they are the only neurons in the cochlear nucleus that do so. In the case of the ELL, there are differences in stimulus selectivity between the maps (11) that are consistent with the conclusions of this paper.