Functional evolution of new and expanded attention networks in humans

Macaque monkeys are often used as a model for the biological basis of human cognition. However, the two species last shared a common ancestor 25 million years ago, and in the intervening time the brain areas underlying cognition have likely evolved along different paths. We examined the similarities and differences of human and macaque brain areas underlying attention, a core cognitive ability, by recording brain activity while subjects of both species performed the same attention-demanding task. We found fundamental differences in the attention-related brain areas in the two species, including the complete absence, in monkeys, of a ventral-attention network present in humans. These results shed light on the evolution of the unique properties of the human brain.

Macaques are often used as a model system for invasive investigations of the neural substrates of cognition. However, 25 million years of evolution separate humans and macaques from their last common ancestor, and this has likely substantially impacted the function of the cortical networks underlying cognitive processes, such as attention. We examined the homology of frontoparietal networks underlying attention by comparing functional MRI data from macaques and humans performing the same visual search task. Although there are broad similarities, we found fundamental differences between the species. First, humans have more dorsal attention network areas than macaques, indicating that in the course of evolution the human attention system has expanded compared with macaques. Second, potentially homologous areas in the dorsal attention network have markedly different biases toward representing the contralateral hemifield, indicating that the underlying neural architecture of these areas may differ in the most basic of properties, such as receptive field distribution. Third, despite clear evidence of the temporoparietal junction node of the ventral attention network in humans as elicited by this visual search task, we did not find functional evidence of a temporoparietal junction in macaques. None of these differences were the result of differences in training, experimental power, or anatomical variability between the two species. The results of this study indicate that macaque data should be applied to human models of cognition cautiously, and demonstrate how evolution may shape cortical networks.