Hemispheric specialization

As extensively reviewed by Bradshaw and Rogers (1993), throughout the animal kingdom there are many behavioral processes that are supported better by one than the other cerebral hemisphere. Obviously, the time delay noted for intercommunication in larger brains is not the only factor contributing to this lateralization. The efficiency achieved by performing computations within closely adjacent neuronal populations likely provides further pressure in this direction, as does the fact that effective interhemispheric communication, rather than simply being slow, may be essentially lacking in certain instances (see Doty, 1989; Doty and Ringo, 1994; Ringo et al., 1994), thus encouraging or necessitating the local solution.

There is a variety of specializations, ranging from paw or hand preference to attention (see below) to very high levels of analysis, such as recognition of faces or species-specific calls. The more pertinent here are those that seem to adumbrate the human situation, where across the population there is a high degree of similarity as to which hemisphere is specialized for which function. Such uniformity is generally lacking for handedness in nonhuman species.

The left hemisphere in birds is strongly specialized for production and interpretation of species- and individual-specific song (see Bradshaw and Rogers, 1993); and the same seems to be true in mice of either sex responding to calls of pups (Ehret, 1987; Ehret and Koch, 1989). Two Japanese macaques (Macaca fuscata) likewise displayed a slight (p < 0.05) right ear, presumably left hemisphere, advantage in recognizing species-specific calls, in contrast with a M. nemestrina and a M. radiata that were equally accurate but showed no bias to one or the other ear (Petersen et al., 1984) for the M. fuscata calls.

The question of hemispheric specialization for analysis of visual material by macaques has received somewhat more attention. As far as discriminating and remembering a wide variety of patterned visual inputs is concerned, there appears to be no difference between the hemispheres (Doty, Ringo, and Lewine, 1988, 1994; Hamilton, 1990). Some of the data suggest that for particularly difficult tasks the left hemisphere may have an advantage (Hamilton and Vermeire, 1991; Lewine, Doty, Astur, and Provencal, 1994), but it is not yet clear whether such an effect is truly independent of the type of visual material or problem with which the animal must cope.

The important discovery is not only that the majority of macaques display hemispheric specialization for certain problems, but also that there is a complementarity— that each hemisphere is uniformly better at one type of problem than another (Hamilton and Vermeire, 1988, 1991; Vermeire, Hamilton, and Erdmann, 1998). In 25 split-brain animals (optic chiasm, anterior commissure, and corpus callosum all transected, allowing each hemisphere to be tested separately by closing one eye), they found only three that had a very slight right hemisphere superiority for discriminating the orientation of lines, the others all being better, commonly much better, when using the left hemisphere (p < 0.001). Correspondingly, in 22 of the same animals, 18 showed a generally robust superiority with the right hemisphere in categorizing the facial expression of their conspecifics, despite the fact that the stimuli were provided by different individuals (again p < 0.001). It could be shown that these specializations were independent in the two hemispheres, that is, that excelling with one type of material in one hemisphere had no significant effect on the presence or absence of type of superiority in the other. About three fourths of the animals, however, showed the full differentiation: left hemisphere best for line orientation, right for facial and emotional recognition. The differentiation was strongest in females.

One of the attractions of these data of Hamilton and Vermeire is that right hemispheric specialization for face recognition is congruent with human findings (e.g., Carey, 1981; Sobotka, Pizlo, and Budohoska, 1984; Diehl and McKeever, 1987; Barrett, Rugg, and Perrett, 1988; Sergent and Signoret, 1992; Mertens, Siegmund, and Griisser, 1993). Although Overman and I (1982) failed in an attempt to show that macaques, as did human subjects, would find the right half of a face more representative of a face than the left, this is scarcely a crucial test. A bit more fundamental is the experiment of Heywood and Cowey (1992), although not directly addressed to the issue of hemispheric specialization. They performed a bilateral extirpation of the cortex in the macaque temporal lobe that has been repeatedly found to contain a substantial population of neurons specifically responsive to faces. However, the animals showed little or no problem with facial recognition, while human prosopagnosic patients had difficulty with many of the stimuli employed. This suggests that the homolog of the human cortical area that is most responsible for facial recognition has still to be identified in macaques.

With two split-brain macaques we (Doty et al., 1999) endeavored to confirm and extend the findings of Hamilton and Vermeire but using a more demanding mnemonic task. The animals were required to identify whether an item was new or had been seen previously (old) in the session of 142 trials, with up to three images intervening between the new and old items. Ocular fixation on a small target centered above the image signaled new, and fixation on a lower target signaled old. The laterality of fixations during examination of each image was used to indicate which hemisphere was in control of the viewing when both eyes were open. Initially, there was no significant difference between the hemispheres of either animal in remembering colored, nonobjective images or human faces, but both showed a right hemispheric superiority for remembering macaque faces, precisely as Vermeire, Hamilton, and Erdmann (1998) had shown.

The male animal was then eliminated, but work continued with the female. To our total surprise the hemispheric dominance, some 15 months after surgery and start of testing, shifted entirely to the left hemisphere, probably as a gradual shift, but its unexpectedness left us unprepared to define its progression. This change was true for superiority in remembering human faces and nonobjective images as well as the macaque faces that were originally better remembered by the right hemisphere. The left hemispheric superiority was reflected not only in the accuracy of performance but also in the pattern of eye fixations during examination of the presented item (Kavcic, Fei, Hu, and Doty, 2000). This unequivocal change in predominance of one hemisphere over the other cautions that one may not—in any case, with macaques—be dealing with hemispheric specialization per se. Rather, it may be a question of meta-control (Levy and Trevarthen, 1976), that is, which hemisphere endeavors to assume behavioral control in a given situation. Hellige (1993), for instance, has demonstrated in human subjects that it is not always the most appropriately specialized hemisphere that controls the response. It is quite possible in the case of this reversal of hemispheric specialization just described that the only specialization is that of controlling the response, even when the now-dominant hemisphere is not viewing the to-be-remembered image. In other words, even when only one hemisphere is viewing an item, the other may intrude by endeavoring to control the response (see Chiarello and Maxfield, 1996). This possibility is indeed suggested by the fact that in the present case, reversing a superiority of performance from the right to the left hemisphere, the performance of the previously superior right hemisphere did, in fact, significantly diminish (Doty et al., 1999).

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