Dissociation of vertical and horizontal components of somesthetic orientation-localization during recovery from cortical damage: Implication regarding central associative functions

Abstract

Blindfolded cats in which SII and adjacent areas had been ablated were tested for their ability to locate cutaneous stimuli as demonstrated by their bringing the mouth into contact with the stimulated point. During recovery, seven cats went through a phase in which they displayed dissociations of the vertical and horizontal components of the orientation-localization movement: either they moved the head downward before initiating any lateral movement or they turned towards the side of stimulation well before achieving accurate proximodistal localization. Hypotheses are offered about which aspects of anatomy and physiology are involved in proximodistal and lateral localization, and a simple mathematical model is given to suggest that one reason why such central associative functions in movement may have evolved is because they require fewer neurons than an alternative conceivable design.Two reciprocally related behavioral phenomena unexpectedly were observed during an experiment designed to measure the effects of cortical ablations on speed and accuracy of the cutaneous orientationlocalization movement and on learned cutaneous behavior. These phenomena suggest that, in the organizational scheme for the normal orientation-localization response, there are distinguishable components, or functions.Even some simpler reflexesrequire participation of higher levels of the nervous system. For example, in contact placing, a tactile stimulus to the surface of the cat's forelimb elicits a coordinated movement involving motion of the same limb in the direction of the stimulus. Physiological and behavioral studies suggest that this response depends on the overlapping SI and MI maps on the sigmoid gyrus (Amassian, Ross, Wertenbaker, & Weiner, 1972;Glassman & Glassman, 1977;Villablanca, Marcus, Olmstead, & Avery, 1976;Welt, Aschoff, Kameda, & Brooks, 1967).Orientation towards stimulated points on the body surface also requires stereotyped stimulus-response relationships, but the neural wiring problem for orientation-localization is more complex than that for contact placing because the muscles needed to This study was supported in part by a grant from the National Science Foundation. I thank Doris E. Cook and Jill R. Olassman for their excellent histological work. Correspondence should be addressed to: Robert B. Glassman, Department of Psychology, Lake Forest College, Lake Forest, Illinois 6004S. 47 move the cat's face towards a stimulated point on the body are not, in general, near that point. Moreover, the relative contributions to the movement by members of the same set of muscles vary depending on which point is stimulated.Behavioral and physiological data have indicated that the following brain areas are among those that participate in orientation-localization behaviors:

Theoretical Note Parsimony in neural representations: Generalization of a model of spatial orientation ability

“…Therefore, left versus right turning could simply follow the overall central neural asymmetry of diffusely summed cutaneous input activity, regardless of the fine spatial distribution of inputs to the topographic maps of either hemisphere. Behavioral evidence is consistent with this hypothesis (Glassman, 1983).…”

“…While cats were behaviorally recovering from unilateral damage to SII cortex and adjacent areas, many were unexpectedly observed to pass through a stage in which the vertical and horizontal orientational movements were largely dissociated. For example, when the cutaneous stimulus was applied to the left forepaw, in some cases the blindfolded cat pitched its head downward to paw level before initiating any leftward movement; in other cases, the lateral movement occurred before the vertical component (Glassman, 1983).…”

A connectionist model of path integration with and without a representation of distance to the starting point

“…One unit stands for forward movement, the other two for (respectively) left (ccw) and right (cw) rotation. This dissociation of movement into translational and rotational components reflects observations of a similar dissociation into polar components in the nervous circuitry controlling head movement in the barn owl Tyto alba (Masino & Knudsen, 1990) and in the cat (Glassman, 1983), as well as whole-body movement in the frog Rana pipiens (Kostyk & Grobstein, 1987;Masino & Grobstein, 1989) and in the rat (Chen, Lin, Green, Barnes, & McNaughton, 1994a, 1994b. All three units have linear responses proportional to the magnitude ofthe rotation and translation during the current step (for details, see the Appendix).…”