THE USE OF VOCALIZATIONS, such as grunts, songs or barks, is extremely common throughout the animal kingdom. Nevertheless, humans are the only species in which these vocalizations have attained the sophistication and communicative effectiveness of speech. How did our ancestors become the only speaking animals, some tens of thousands of years ago? Did this change happen abruptly, involving the sudden appearance of a new cerebral region or pattern of cerebral connections? Or did it happen through a more gradual evolutionary process, in which brain structures already present to some extent in other animals were put to a different and more complex use in the human brain?
A recent study in Nature Neuroscience yields critical new information, uncovering what could constitute the “missing link” between the brain of vocalizing nonhuman species and the human brain: evidence that a cerebral region specialized for processing voice, known to exist in the human brain, has a counterpart in the brain of rhesus macaques.
Neuroscientist Christopher I. Petkov of the Max Planck Institute for Biological Cybernetics in Tbingen, Germany, and his colleagues used functional magnetic resonance imaging to explore the macaque brain. They measured cerebral activity of awake monkeys that were listening to different categories of natural sounds, including macaque vocalizations. The researchers found evidence for a “voice area” in the auditory cortex of these macaques: a discrete region of the anterior temporal lobe in which activity was greater for macaque vocalizations than for other sound categories.
This region was observed in several individuals, even under the condition of total anesthesia. More surprising, the region showed repetition-induced reduction of activity—or neuronal adaptation—in response to different calls coming from the same individual. This finding suggests that this brain region processes information about the identity of the speaker, a phenomenon that is also observed in the human voice area.
Long History of Voice?
Perhaps the most remarkable implication of these findings is that the voice area previously identified in the human brain is not uniquely human and that it has a counterpart in the brain of nonhuman primates. That discovery, in turn, implies that the voice area has a long evolutionary history and was probably already present in the common ancestor of macaques and humans some 20 million years ago. It is known that the cognitive talents underlying voice perception, such as speaker recognition, are shared with many other animal species, but the findings of Petkov and his colleagues provide a cerebral location for these abilities.
Ironically, most of the research into the evolutionary basis of language has focused so far on a single function—speech perception—which is unique to humans, and thus evolutionary precursors are hard, if not impossible, to identify. The present findings hint at another, possibly more rewarding, strategy: perhaps looking at what we have in common with other animals—that is, a rich cerebral substrate to process vocalizations and extract speaker-related information—will allow us to understand the evolution of speech. Indeed, Petkov’s findings indicate that when our ancestors began to talk, they already were equipped with sophisticated neural machinery specialized in voice processing.
Another important implication of Petkov’s findings concerns the functional lateralization of the macaque voice area. A well-established property of the human cerebral substrate for speech (particularly speech production) is its lateralization to the left hemisphere. This known asymmetry has led researchers to investigate whether a similar left-hemispheric bias could be found in other animals, as a possible evolutionary precursor of human language. Unfortunately, this long-standing belief has possibly resulted in a strong bias in the literature, whereby studies uncovering any leftward asymmetry in nonhuman primates are much more likely to be published in leading journals.
A Role for the Right
A counterintuitive but essential feature of Petkov’s results, similar to the corresponding findings in the human brain, is that voice-selective activity was stronger in the right hemisphere. Furthermore, the identity-specific neuronal adaptation was observed only in the right hemisphere of the macaque brain, exactly as in the human studies. This finding means that the right hemisphere may well have played a major role in how speech appeared in our ancestors and that a response to the puzzle of speech evolution may lie not only in the left hemisphere.
We have much work ahead before we can attain a complete understanding of the functional role of the voice area, in macaques as well as in humans. Several alternative hypotheses remain to be tested: Does the voice area represent a hardwired preference for the particular acoustical structure of vocalizations from one’s own species? Or is it more simply a “formant” detector, a structure specialized in detecting vocal features in general? Another possibility is that this voice area is actually a “social” structure, tuned to vocalizations because they are cues for social interaction and not because they share a particular acoustical structure.
In conclusion, Petkov’s findings provide an exciting common substrate for high-level, or complex, auditory cognition that can be studied in parallel in humans and in macaques. Now that the location of the voice area in the macaque brain has been established, researchers will obtain critical additional information in the near future by exploring the monkey’s voice area using more conventional electrophysiological techniques, such as recording directly from neurons. Even more important, this seminal work opens the road for comparative neuroimaging studies in which humans and other animals perform similar tasks using similar methodologies, and the results can be analyzed using similar strategies.
Note: This story was originally published with the name, "Monkeys Hear Voices".