Evolution amplified processing with temporally dispersed slow neuronal connectivity in primates

Abstract

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...

The Crossed Projection to the Striatum in Two Species of Monkey and in Humans: Behavioral and Evolutionary Significance

“…In the monkey, the delays from prefrontal cortex are 3.4 ms for the ipsilateral (Innocenti et al 2013) and 5.1 ms for the contralateral projection to n caudatus (this paper). By taking into account an increase in axon diameters in humans in the order of 30% (compatible with macaque/human comparative data; Caminiti et al 2009) and of conduction distance proportional to the cubic route of brain volumes, validated by DT tracing (Caminiti et al 2009) the ipsi-and contra-calculated values in humans are 6.6 and 9.9 ms ( Table 2). This means an average difference of 3.3 ms between the ipsilateral and the contralateral projection.…”

“…The third (M93-80) from the Cognition Center, University of Fribourg, was a male of 4 years of age (4.5 kg body weight). Other connections of the first 2 monkeys were published (Caminiti et al 2009;Tomasi et al 2012;Innocenti et al 2013) and the methods reported therein. Briefly, surgery was performed by a professional human neurosurgeon under strict sterile conditions.…”

“…Section thickness was 34 μm. Sections were reacted for BDA, and alternated sections were counterstained with cresyl violet or with the Gallyas method for myelin as in Caminiti et al (2009).…”

“…Since BDA tracing allowed to estimate the diameter and length of the axons, the conduction velocities and delays they generate can be calculated (Caminiti et al 2009;Tomasi et al 2012;Innocenti et al 2013). Comparing the delays in the ipsilateral versus contralateral cortico-striatal projection might provide an answer to the question: "why a cortico-striatal callosal projection?"…”

“…Notice also that the projections extend to the isthmus of the CC and anterior splenium in humans, not in monkeys. (Caminiti et al 2009)) and of conduction distance proportional to the cubic route of brain volumes. The ipsi-and contra-calculated values thus obtained in humans are 6.6 and 9.9 ms ( Table 2).…”