Conflict and integration of spatial attention between disconnected hemispheres
The article by Dr Ishiai and colleagues1 contains a critical piece of anatomical data (that is, the “sparing of the rostrum and the inferior half of the genu” (fig 1)) which has been ignored by the respected authors as to its probable role in underpinning the results they reported. This may have occurred because of their conventional theoretical perspective on motor control in the human, in the light of which such matters might be afforded. However, the doctrine of contralaterality of movement control (CMC) in humans has been recently revised2 to account for observations such as theirs in the sensory realm, as well as others in the motor realm that underpin the classical laterality indexed trilogy of contralateral hemiplegia/ipsilateral apraxia (with and without speech deficit); ipsilateral (non-dominant) weakness in lesions affecting the major hemisphere; and non-dominant weakness in lesions affecting the callosum.
The one-way callosal traffic theory (underpinning lateralities of executive functions) states that all voluntary actions involving the non-dominant hand entail a sequential activation (that is, major followed by minor hemisphere, mediated through the callosum) of a devoted neuronal aggregate distributed between two hemispheres. The commands for the effectors on the dominant side reach them directly whence they arise. Those for the non-dominant effectors traverse the callosum.
Evidence favouring this scheme is overwhelming, as detailed elsewhere.2 Thus the improvement of performance seen upon the voluntary movement of the non-dominant side reflected the activating effect on both hemispheres when the left hand moved voluntarily, temporarily “lightening up” the dormant right hemisphere through the remaining functioning callosal connections depicted on MRI. The new scheme, therefore, bypasses the controversies mentioned by the authors.
It is to be noted that this scheme relates to all movements, whether cranial (such as eye movements) or appendicular. Anyone in doubt of the veracity of this claim can find solace when they hear a double click upon snapping their fingers simultaneously, instead of one click mandated by CMC doctrine , with the second click arising from the neural (as opposed to ostensible) non-dominant hand (Derakhshan I, unpublished data). The callosal delay imposed on the non-dominant hand has been known for 160 years, under the name Melody Lead of the right hand of piano players, and is thought to represent artistic expression.3 Its range, however, (10–40 ms) makes that interpretation highly unlikely. Callosal delay when turning the eyes to the non-dominant side has long been documented.4 However, for the reasons alluded to earlier, more modern workers have ignored it, some calling it “idiosyncratic,”5 an interpretation inconsistent with the consistency it shows itself when sufficient data are given.5
References
Authors’ reply
- 2Department of Rehabilitation, Tokyo Metropolitan Institute for Neuroscience, 2-6 Musashidai, Fuchu City, Tokyo 183-8526, Japan
- 3Department of Neurology, Kawaguchi Kogyo General Hospital, 1-18-15 Aoki, Kawaguchi City, Saitama 332-0031, Japan
As Dr Derakhshan points out, MRI showed that the callosal lesion of our patient spared the rostrum and the inferior half of the genu. In our paper, we did not comment upon the role of partially spared callosal fibres in the dissociated line bisection performance between the right and left hands. At least in the sphere of praxis, the dominant left hemisphere hardly seemed to contribute to the control of the left hand, as our patient showed severe apraxia of this hand. However, the use of the non-dominant left hand to bisect a line would possibly have activated the ipsilateral left hemisphere as well as the contralateral right hemisphere, because of command transmission through the spared callosal fibres. If so, why would the use of the right hand not activate the ipsilateral right hemisphere enough to correct biased bisection to the right side? Derakhshan seems to rely on the role of the left hemisphere in motor control and praxis to explain the dissociated performance according to the laterality of hand use.
As for directed attention, the right hemisphere is considered to play a major role,1,2 although Derakhshan’s explanation needs no such hemispheric dominance. If, however, this widely accepted hypothesis is applied to his command transmission explanation through the partially spared callosum, the use of the right hand would activate not only the left “spatially non-dominant” hemisphere but also the right “spatially dominant” hemisphere. In our patient, rightward errors with the right hand were observed after repetitive bisection of the lines, and leftward searches (contralateral to the error direction) almost always occurred after placement of the subjective midpoint. The latter finding was considered to represent an interhemispheric conflict of attention. By contrast, accurate bisection with the left hand was achieved after a few trials in which leftward placement of the mark was followed by one or two rapid rightward searches contralateral to the displacement. This rapid improvement might be explained by transmission of attentional information through the spared callosal fibres. However, we prefer to reject that explanation, as interhemispheric callosal transmission should be bidirectional.
While the right hand and the left hemisphere bisected a line, the left visual field and the right hemisphere perceived the longer extent to the left of the fixation at which the mark was later placed. We do not consider that such perception of the right hemisphere was transmitted to the left hemisphere through the subcortical neural connection. In patients with callosal disconnection, the gaze direction is unitary, and the direction and distribution of attention may be integrated under most ordinary conditions.3 When responding with the left hand, the right hemisphere may integrate attention to the extent perceived in the left and right visual fields. The capacity of the “intact” left hemisphere to integrate spatial attention remained to be explored, as our patient had extracallosal lesion in the subcortical white matter of the cingulate gyrus.
