The cerebral cortex is the largest and most intricately connected part of the mammalian brain. Its size and complexity has increased during the course of evolution, allowing improvements in old functions and causing the emergence of new ones, such as language. This has expanded the behavioural and cognitive repertoire of different species and has determined their competitive success. To allow the relatively rapid emergence of large evolutionary changes in a structure of such importance and complexity, the mechanisms by which cortical circuitry develops must be flexible and yet robust against changes that could disrupt the normal functions of the networks.
The corpus callosum (CC) provides the main route of communication between the 2 hemispheres of the brain. In monkeys, chimpanzees, and humans, callosal axons of distinct size interconnect functionally different cortical areas. Thinner axons in the genu and in the posterior body of the CC interconnect the prefrontal and parietal areas, respectively, and thicker axons in the midbody and in the splenium interconnect primary motor, somatosensory, and visual areas. At all locations, axon diameter, and hence its conduction velocity, increases slightly in the chimpanzee compared with the macaque because of an increased number of large axons but not between the chimpanzee and man. This, together with the longer connections in larger brains, doubles the expected conduction delays between the hemispheres, from macaque to man, and amplifies their range about 3-fold. These changes can have several consequences for cortical dynamics, particularly on the cycle of interhemispheric oscillators.axons ͉ cerebral cortex ͉ corpus callosum ͉ information transfer ͉ interhemispheric T he increased size of the human brain and its anatomical asymmetry and functional lateralization suggest that connections between the hemispheres must have undergone a substantial degree of reorganization in primate evolution. The timing of interhemispheric interactions is probably a crucial constraint in this reorganization (1). However, although some data suggest a progressive slowing down of interhemispheric communication in larger brains (1, 2), other data maintain that the speed of interhemispheric communication scales with brain size (3, 4). In this study, we examined interhemispheric connections in the macaque, chimpanzee, and human. The results reconcile the 2 views presented above and open unique perspectives on the role of long corticocortical connections in cortical dynamics and computation. ResultsIn cross-sections of the chimpanzee corpus callosum (CC), the intensity of myelin staining was found to vary in the anterior-toposterior direction, suggesting that larger and more myelinated axons would be found in the middle of the body and in the anterior part of the splenium. Indeed, the diameter of axons was found to increase progressively from anterior to the midbody and to decrease again further posterior [supporting information (SI) Fig. S1]. Thicker axons were also found in the anterior and lower part of the splenium. This pattern resembled that described in the macaque (5) and human (6) CC.To understand if the differences in axonal size relates to the origin of the CC axons, as suggested by LaMantia and Rakic (5), in 3 long-tailed macaques (Macaca fascicularis), 9 cortical sites (prefrontal, premotor, somatosensory, parietal, and visual areas) were injected with biotinylated dextran amine (BDA) (Fig. 1 A and B).Each injection labeled a discrete cluster of axons in the CC. As expected from previous anatomical (7,8) and imaging (9) work, the position of the axonal clusters in the CC corresponded to the anteroposterior location of the injection...
Three macaque monkeys and 13 healthy human volunteers underwent diffusion tensor MRI with a 3 Tesla scanner for diffusion tract tracing (DTT) reconstruction of callosal bundles from different areas. In six macaque monkeys and three human subjects, the length of fiber tracts was obtained from histological data and combined with information on the distribution of axon diameter, so as to estimate callosal conduction delays from different areas. The results showed that in monkeys, the spectrum of tract lengths obtained with DTT closely matches that estimated from histological reconstruction of axons labeled with an anterogradely transported tracer. For each sector of the callosum, we obtained very similar conduction delays regardless of whether conduction distance was obtained from tractography or from histological analysis of labeled axons. This direct validation of DTT measurements by histological methods in monkeys was a prerequisite for the computation of the callosal conduction distances and delays in humans, which we had previously obtained by extrapolating the length of callosal axons from that of the monkey, proportionally to the brain volumes in the two species. For this analysis, we used the distribution of axon diameters from four different sectors of the corpus callosum. As in monkeys, in humans the shortest callosal conduction delays were those of motor, somatosensory, and premotor areas; the longer ones were those of temporal, parietal, and visual areas. These results provide the first histological validation of anatomical data about connection length in the primate brain based on DTT imaging.
The sexual dimorphism of the human corpus callosum (CC) is currently controversial, possibly because of difficulties in morphometric analysis. We have reinvestigated the issue by using morphometric techniques specially designed to yield objective measurements of CC size and shape. The development of the CC was studied with similar techniques in order to investigate whether its final shape and size might be influenced by axonal elimination, as could be expected from previous animal studies. We have measured the CCs of 32 men and 26 women; 27 male and 19 female CCs were from brain tissue, the others were from magnetic resonance imaging graphs. Women tended to have 1) a smaller cross-sectional callosal area (CCA); 2) a larger fraction of CCA in the posterior fifth of the CC; 3) more slender CCs; and 4) more bulbous splenia. These differences could not be detected by simple inspection but were demonstrated by measurement and statistical analysis. However, CCA was correlated with the other sexually dimorphic parameters, and the sex-related differences in the latter became nonsignificant when variations in CCA were factored out or when male and female populations with similar CCA were compared. In addition, we analyzed CCs of 16 male and 16 female fetuses and of 13 male and 15 female infants and children. This sample ranged in age between 20 weeks of gestation and 14 years but covered in detail the period up to 14 months after birth. CCA increased throughout the latter period but decreased slightly between about 33 weeks of gestation and the beginning of the second postnatal mouth. This decrease coincided with thinning of the CC and a marked increase in bulbosity of the splenium. No sexual dimorphism could be demonstrated until the beginning of the postnatal period. In the age group between birth (at term) and the 14th month, CCA was, as in the adult, larger in males. Unlike in the adults, the CC was longer in males and the bulbosity index was the same in the two sexes. Axonal elimination may play a role in the perinatal pause in CCA growth and in the concomitant changes in callosal shape.
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