I believe (but cannot prove) that we vastly underestimate the differences that set the human brain apart from the brains of other primates.
Certainly, no one can deny that there are important similarities in the overall layout of the human brain and, say, the macaque monkey brain. Our primary sensory and motor cortices are organized in similar ways. Even in higher brain areas, homologies can be found. In the parietal lobe, using brain-imaging methods, my lab has observed plausible human counterparts to several areas of the macaque brain, involved in eye movement, hand gestures, and even number processing.
Yet I fear that those early successes in drawing human-monkey homologies tend to mask other massive differences. If we compare the primary visual areas of macaques and humans, there is already a two-fold difference in surface area, but in parietal and frontal areas, a twenty-to fifty-fold increase is found. Even such a massive distortion may not suffice to "align" the macaque and human brain. Many of us suspect that, in regions such as the prefrontal and inferior parietal cortices, the changes are so dramatic that they may amount to the addition of new brain areas.
At a more microscopic level, it is already known that there is a new type of neuron which is found in the anterior cingulate region of humans and great apes, but not in other primates. These "spindle cells" send connections throughout the cortex, and thus contribute to a massive increase in long-distance connectivity in the human brain. Indeed, the change in relative white matter volume is perhaps what is most dramatic about the human brain.
I believe that these surface and connectivity changes, although they are in many cases quantitative, have brought about a qualitative revolution in brain function:
Breaking the brain's modularity.
Jean-Pierre Changeux and I have proposed that the increased connectivity of the human brain gives access to a new mode of brain function, characterized by a very flexible communication between distant brain areas. We may possess roughly the same list of specialized cerebral processors as our primate ancestors. However, I speculate that what might be unique about the human brain is its capacity to access the information inside each processor, and make it available to almost any other processor through long-distance connections. I believe that we humans have a much more developed conscious workspace—a set of brain areas that can fluidly exchange signals, thus allowing us to internally manipulate information and to perform new mental syntheses. Using the workspace's long-distance connections, we can mobilize, in a top-down manner, essentially any brain area and bring it into consciousness.
Spontaneous activity and the autonomy of consciousness.
Once the internal connectivity of a system exceeds a threshold, it begins to be dominated by self-sustained, reverberating states of activity. I believe that the human workspace system has passed this threshold, and has gained a considerable autonomy relative to the outside world. The human brain is much less at the mercy of signals from the outside world. Its activity never ceases to reverberate from area to area, thus generating a highly structured spontaneous flow of thoughts that we project on the outside world.
Of course, spontaneous brain activity is present in all species, but if I am correct we will discover that it is both more evident and more structured in the human brain, at least in higher cortical areas where "workspace" neurons with long-distance axons are denser. Furthermore, if human brain activity can be detached from outside stimulation, we will need to find new paradigms to study it, because bombarding the human brain with stimuli, as we do in most brain-imaging experiments, will not suffice. There is already some evidence for this statement: by directly comparing fMRI activations evoked by the same visual stimuli in humans and macaques, Guy Orban and his colleagues in Leuven have found that prefrontal cortex activity is five times larger in macaques than in humans. In their own words, "there may be more volitional control over visual processing in humans than in monkeys".
The profound influence of culture on the human brain.
The human species is also unique in its ability to expand its functionality by inventing new cultural tools. Writing, arithmetic, science, are all very recent inventions—our brains did not have time to evolve for them, but I speculate that they were made possible because we can mobilize our old areas in novel ways. When we learn to read, we "recycle" a specific region of our visual system, which has become known as the "visual word form area", for the purpose of recognizing strings of letters and connecting them to language areas. When we learn Arabic numerals, likewise, we build a circuit to quickly convert those shapes into quantities, a fast connection from bilateral visual areas to the parietal quantity area. Even an invention as elementary as finger counting changes dramatically our cognitive abilities: Amazonian people that have not invented counting are unable to make exact calculations as simple as 6-2.
Crucially, this "cultural recycling" implies that whenever we look at a human brain, the functional architecture that we see results from a complex mixture of biological and cultural constraints. Education is likely to greatly increase the gap between the human brain and that of our primate cousins. Virtually all human brain imaging experiments today are performed on highly literate volunteers—and therefore, presumably, highly transformed brains. To better understand the differences between the human brain and the monkey brain, we will need to invent new methods, both to decipher the organization of the baby brain prior to education, and to study of how it changes with education