Controversies in NeuroscienceTopographic Maps are Fundamental to Sensory Processing
Introduction
We have long known that orderly representations of the sensory surfaces exist in cortex and other parts of the brain. Early evidence for these maps came from electrical stimulation of the cortex (e.g., [54]), sequences of sensation, or movement in focal epilepsy (e.g., [38]), and impairments after restricted cortical lesions [35], but the details and more compelling evidence came only after surface electrode, and then microelectrode stimulation and recording techniques came into common use. Adrian [2]and Woolsey (e.g., [55]) were in the forefront of those recording from the cortex and demonstrating somatotopic maps. These approaches have been applied to the auditory and visual systems, and numerous cortical and subcortical representations of the cochlea, retina, and body surface have been described (see 5, 26, 29, 45, 57, 58, 67). Subcortical and cortical representations reflect the order of the receptor sheet with the greatest fidelity in structures early in the hierarchy of processing stations (see [26]). At higher levels, neurons acquire larger receptive fields, and somatotopic, cochleotopic, and retinotopic organizations become less apparent or possibly lost.
Opinions about the meaning of topographic order have varied. Some investigators, especially those involved in disclosing the order of cortical maps, regarded the topographic patterns as essential for sensory discrimination. The arguments were made, for example, that the spatial separation of foci of neural activity in the cortical maps was the basis for localizing and distinguishing stimuli as separate on the body (see [72]). Others seemed to have held that whatever order exists in sensory maps is of little significance, and that such order should disappear as soon as possible in sensory hierarchies. Hebb [34], for example, reflected a common view when he stated that after area 18 āall topological organization in the visual system seems to have disappeared.ā Doty [20]once concluded that āthe topographical arrangement of the retinocortical projection is in itself of minor or no importance in the visual analysis of geometric patterns.ā Likewise, the tonotopic organization in auditory cortex once was viewed as weak, at best, and unimportant for cortical functions (e.g. [24]). A widespread early view was that topographic organization is detrimental or incompatible with the presumed associative functions of cortex (for review, see [57]). In contrast, the now widely held opinion is that the topographic features of cortical and subcortical maps are not incidental, but essential to much brain function.
Section snippets
The Nature of Brain Maps
Until recently, we had little experimental evidence on the organization of most of the neocortex. The cortical sensory fields were thought to be few in number, and most of the cortex was thought to be associational and multimodal, and thus unlikely to have any topographic organization (see [57]). We now know that even mammals with little neocortex and few subdivisions devote much of this cortex to maps of sensory surfaces (see [46]). For example, marsupial opossums, with very little neocortex,
The Development of Brain Maps
Somatotopic and other isomorphic maps of receptor surfaces are thought to emerge in development through a process of matching of inputs with targets based on molecular recognition (see [73]) followed by an activity-dependent local sorting of terminals (see [48]). The molecular matching creates the topographic representations within structures throughout processing hierarchies, while the local selection of synapses and connections, based on the strengthening effects of temporal correlations and
The Evolution of Map Structure
Existing structures and behaviors have been subjected to selection over alternative structures and behaviors in evolution. While selection would seem to push structures toward optimal design, this can occur only within the constraints of the system. As a sometimes stated example, wheels may be the best structure for locomotion on hard, flat surfaces, but biologically, wheels are difficult to create. Thus, the optimal design often may not be possible. As suggested above, another consideration is
The Argument of Good Design
Why are the maps topographical and why so many? A major answer for both questions is that it is good biological design (see [62]) to have both topography within areas, and have multiple areas. We presume that a fundamental operation of local circuits within sensory systems is to make context-dependent comparisons. Biologically important information often results from an assessment of how input coming in from one focus of receptors is different from that coming in from adjoining sets of
The Argument that Perception is Based on Topographic Maps
One type of argument for the functional importance of topographic maps is based on parallel relationships between map structure and perception. Adrian [1]illustrated this type of relationship long ago when he pointed out that the decay in the discharge of a cutaneous afferent to a maintained stimulus reflected the decay in the magnitude of sensation, and thus the sensation must be based on the discharge rate. A similar type of reasoning followed when Adrian [2]showed that the parts of
A Counter Argument
A major argument against the view that topographic maps are functionally significant is that lesions often do not produce the expected consequences. When Doty [20]argued that the topographic organization of visual cortex was of āminor or no importance,ā he did so because it seemed that lesions that disrupted the topography had so little effect on visual performance. Lashleyās [53]well-known conclusions based on the effects of lesions on visual performance in rats were similar. Investigators
Conclusions
- 1.
Topographic maps of receptor surfaces occupy much of neocortex of all mammalian species. This suggests that they are important.
- 2.
To the extent that such maps emerge in development as a result of an interaction between relatively few factors, map features may be linked. Thus, all features of maps may not be adaptive or have useful functional consequences.
- 3.
Topographical maps effectively group neurons that most commonly interact, thus decreasing requirements for long, slow, and metabolically costly
Acknowledgements
Helpful comments on this manuscript were provided by Kyle Cave, Sherre Florence, Leah Krubitzer, and Jeff Schall.
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