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Gasser and Erlanger shared the 1944 Nobel Prize in Physiology and Medicine for their elegant demonstration of a direct relationship between axon diameter and conduction velocity. Their work established that different sensations within a single cutaneous nerve (e.g. pain and temperature versus touch) are transmitted via axons of different calibre. Inspired by their findings, Bishop (1933) demonstrated that axons in the optic nerve can be divided into three main populations according to their conduction velocities and diameters. By analogy to the work of Gasser & Erlanger (1929), Bishop proposed that the three optic nerve axon classes process different sensory qualities. Although Bishop ultimately attributed differences in the diameter of optic nerve axons to phylogenetic age, his original observations continue to be relevant to modern views of parallel processing within the mammalian visual system.
Later work on the cat visual system (reviewed by Stone, 1983) established that retinal ganglion cells and their target cells in the lateral geniculate nucleus (LGN) form three distinct classes generally referred to as W, X and Y. These cell classes differ in morphology, axon diameter, response properties and conduction velocity. Information within each class is kept largely separate from retina to cortex. Thus the large retinal ganglion cells innervate large LGN cells, medium retinal ganglion cells innervate medium LGN cells, and small retinal ganglion cells innervate small LGN cells. The projection from each LGN cell class terminates in a distinct pattern in the cortex.
In primates, only the large-cell magnocellular (M) and the medium-cell parvocellular (P) geniculostriate pathways have been studied in detail. Much less is known about any contribution to visual processing made by the small-cell koniocellular (K) pathway especially in simian primates (see Casagrande, 1994, for overview and Fig. 1). The paper by Solomon et al. (1999) in this issue of The Journal of Physiology is another in a series of elegant studies by this group that has begun to examine the physiology of K LGN cells in simian primates. Their paper demonstrates that most K LGN cells in marmosets respond briskly to grating stimuli, unlike the sluggish responses reported for cat W cells. They also show that, at any given eccentricity, the temporal contrast sensitivity of K cells lies between that of M and P cells. Overall, the response properties of K cells more closely resemble those of P cells than those of M cells. A previous qualitative assessment of receptive field properties by this group revealed that K cells in marmosets represent a functionally heterogeneous group. The results of their investigations with marmosets are consistent with older studies using bush babies that demonstrated that the spatial properties of some K cells are intermediate to those of M and P cells (see Casagrande & Norton, 1991, for details), and that K cells as a group are physiologically heterogeneous when a variety of properties are considered. There are, however, species differences. Some K cells in marmosets and macaque monkeys, for example, respond to colour (blue-ON cells) (White et al. 1998) and the majority of K cells in marmosets respond briskly and exhibit a classical centre/surround organization (Solomon et al. 1999). By contrast, blue cones are absent in the nocturnal primate bush baby, so their K cells lack an input from this cone type. Additionally, many bush baby K cells exhibit a non-traditional receptive field organization and are therefore difficult to drive (reviewed by Casagrande & Norton, 1991). The latter finding also might reflect variation between species, but could be due to a sampling bias since laminar differences in K cell projections have been reported (Ding & Casagrande, 1997).
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The numbered K layers lie between the main LGN layers and next to the optic tract. Note that only two P layers are shown since additional layers seen in some primates represent splits in the P layers within the central vision representation of the nucleus. M/P and K pathways terminate in layers IV and VI, and within the cytochrome oxidase (CO) blobs (represented by small circles) in layers III and I, respectively. Cells in the CO blobs, in turn, project to three cortical areas: V2, the dorsal lateral visual area (DL, also called V4), and the dorsal medial visual area (DM, also called V3/V3a). CO blob target cells in V2 and DL are considered to be part of a hierarchy of areas concerned with object vision. Area DM is considered part of a hierarchy of areas concerned with spatial location and visual motion. c, innervated by the contralateral eye; i, innervated by the ipsilateral eye. See Casagrande & Kaas (1994) for details. | ||
The specific functions of K cells are, at present, still unclear. The data provided by Solomon et al. (1999) in this issue support the idea that K cells in simian primates contribute to 'conventional' aspects of visual processing. However, other data suggest a variety of neuromodulatory roles (see Casagrande, 1994). Similarities in the anatomical connections between K cells in primates and W cells in other mammals further suggest that this pathway subserves some common function across species that remains to be identified. Nevertheless, the early proposals by Gasser, Erlanger and Bishop, that cells with different axon diameters represent functionally distinct cell classes, has been well supported, most recently by the current study of Solomon et al. (1999).
| Bishop, G. H. (1933). American Journal of Physiology 106, 460-470. | |
| Casagrande, V. A. (1994). Trends in Neurosciences 17, 305-310 | [Medline] |
| Casagrande, V. A. & Kaas, J. H. (1994). In Cerebral Cortex, ed. Peters, A. & Rockland, K. S., pp. 201-259. Plenum Press, New York. | |
| Casagrande, V. A. & Norton, T. T. (1991). In The Neural Basis of Vision Function: Vision and Visual Dysfunction 4, ed. Leventhal, A., pp 41-84. Macmillan Press Ltd, London. | |
| Ding, Y. & Casagrande, V. A. (1997). Visual Neuroscience 14, 691-704 | [Medline] |
| Gasser, H. S. & Erlanger, J. (1929). American Journal of Physiology 88, 581-591. | |
| Solomon, S. G., White, A. J. R. & Martin, P. R. (1999). The Journal of Physiology 517, 907-917. | [Abstract/Full Text] |
| Stone, J. (1983). Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision, pp. 83-108. Plenum Press, New York. | |
| White, A. J. R., Wilder, H. D., Goodchild, A. K., Sefton, A. J. & Martin, P. R. (1998). Journal of Neurophysiology 80, 2063-2076 | [Abstract/Full Text] |
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