Two cerebral cortical areas in the left hemisphere are most commonly associated with language functions. The first, commonly referred to as Wernicke’s area, is a receptive region for the processing and integration of auditory sensory information [4
], and the second, known as Broca’s area, is a productive region concerned with the encoding of vocal signals into meaningful words and sentences [5
]. In other words, Broca’s area functions primarily in the planning and execution of speech, whereas Wernicke’s area functions to make sense of the speech that a listener perceives. However, this classic modular view of linguistic processing is now considered somewhat dated [6
], and it is evident that both cortical as well as subcortical structures and circuits play essential roles in speech production and perception [7
]. Notwithstanding, recent data confirm that left lateralization for linguistic processing is functionally significant [9
], modality independent [10
], and is associated not merely with the perception or production of utterances but with their meaning [13
]. It has been suggested that this hemispheric specialization for language evolved from a lateralized manual communication system that arose in a common human and chimpanzee ancestor [14
]. Consistent with this theory are data that indicate that chimpanzees intentionally and referentially communicate via manual gestures [15
] and, like humans, preferentially use their right hand for communicative gestures [17
]. However, more recent data indicate that chimpanzees also use novel sounds to capture the attention of a human and alter the production of their vocal signals as a function of the communicative demands of a situation [18
]. These results suggest that chimpanzees intentionally produce manual gestures as well as vocal signals to communicate with humans, and although these signals are manifest in different modalities, their communicative function is the same.
Human-like left hemisphere neuroanatomical asymmetries also have been identified in both the IFG and the posterior temporal lobe of the chimpanzee brain [20
], regions considered homologous to Broca’s and Wernicke’s areas, respectively. For the IFG, leftward asymmetry is more pronounced in individuals that preferentially produce manual gestures with their right hand compared to those apes that do not show consistent hand use [22
]. Despite this association between hand use for gestures and morphological asymmetries in the chimpanzee IFG, the functional role, if any, of the IFG in chimpanzee communication remains unknown. Indeed, data on the neural systems involved in gestural or vocal production in great apes, most notably chimpanzees, are virtually absent in the scientific literature yet are critical for understanding the evolution of language.
Here, we used positron emission tomography (PET) to examine the neural correlates of the production of communicative gestures and vocal signals in chimpanzees. We chose to focus on communicative signals directed toward humans given that previous research has demonstrated that chimpanzees and other great apes reliably produce manual communicative gestures but only when a human is present and visually oriented toward the subjects [16
]. In addition, chimpanzees (and other great apes) consistently produce vocalizations and other nonvocal acoustic signals, such as hand clapping, as a means of capturing the attention of an otherwise inattentive social agent [16
]. In other words, the production of these communicative signals is initiated by the apes, self-paced, and not bound to a particular context or emotional state.
For this study, three subjects participated in two 40 min behavioral tasks (see Experimental Procedures). Each task began with the subject consuming a radioactive ligand, 18F-fluoro-deoxyglucose (18F-FDG), that had been diluted in a small amount of a sugar-free flavored drink mixture. Subsequently, for the experimental condition (GV), a cache of food was placed outside the subject’s home enclosure with the intermittent presence of a human in order to elicit the production of communicative gestures and vocal signals during the 18F-FDG uptake period. In order to remove the potential influence of general motor actions on PET uptake, the subjects also participated in a second baseline reach and grasp task (BL) in which both the human experimenter and the food were present, but the task did not elicit any communicative behaviors in the apes. In order to isolate the neural correlates of the communicative behaviors, PET data from the BL task were subtracted from the GV task, resulting in a comparison activation (GV > BL). Significant areas of activation (GV > BL) were identified by using paired sample t tests (t ≥ 4.31, p < 0.025; one-tailed test).
All three subjects produced both gestures and vocalizations in the GV task during the 40 min uptake period (see Table S1
available online), although the frequency of vocal production far exceeded that of gestures. Whole-brain analyses revealed significantly greater activation in the GV condition compared with the BL in a number of brain regions (see and and ), including the left IFG and caudate/putamen, bilateral posterior cingulate gyrus and prefrontal cortex, and right lateral cerebellum (not shown in ). To determine if the observed activation in the left IFG and other regions were significantly lateralized, the average comparison volume (GV > BL) for all three subjects was flipped on the left-right axis and subtracted from the correctly oriented volume. Significant lateralized areas of activation (t ≥ 4.31) are depicted in overlaid on the MR image of a representative chimpanzee brain. A comparison of these images with the activations depicted in indicate that the results of the lateralization analysis are largely consistent with the whole-brain data. Specifically, significant lateralized activity was observed in the left IFG, left caudate/putamen, and the right middle frontal gyrus.
Significant Areas of Activation, t ≥ 4.31, for GV > BL
Three-Dimensional Reconstructions of Magnetic Resonance Images of a Representative Chimpanzee Brain
Significant Areas of Activation for Communicative Production
Significant Lateralized Activation
Given the procedural challenges involved with conducting PET with chimpanzees, three subjects were included in our study. This, to some extent, limits the statistical power that would be possible for an individual analysis. Therefore, whole-brain analyses were conducted on the three subjects collectively. The fact that significant areas of activation were identified suggests consistency in activation among the subjects. However, for illustrative purposes, standardized whole-brain PET activations from each individual subject (GV > BL) overlaid on an MR image of a representative chimpanzee brain are available online as supplemental movies
These results suggest that subcortical and neocortical areas are active concurrently during the production of communicative manual gestures and vocal signals in chimpanzees—a finding that bears some similarities to the neural mechanisms involved in the production of language [7
]. Recent studies in macaque monkeys have reported asymmetric activity of cortical regions after passive listening to conspecific vocalizations including the proposed Broca’s area homolog ([29
], but see [31
] for a critique). However, these studies did not examine the production of communicative signals by the monkeys. Previous research that has focused on vocal production in monkeys found that cortical lesions to the neuroanatomical homolog of Broca’s area had no effect on vocal behavior [32
], although stimulation of this area does result in orofacial movements in macaque monkeys [34
]. The fact that chimpanzee communicative signaling activates both subcortical and cortical structures, in conjunction with data that indicate these signals are referential and produced intentionally, suggests that the precursors to human language are present at both the behavioral and neuroanatomical levels.
It is important to note that during the uptake period, the chimpanzee subjects produced manual gestures as well as a variety of vocal signals. Therefore, the independent effects of these communicative signals on neural metabolic activity cannot be isolated. Pragmatically, this is challenging because the co-occurrence of gestures and vocalizations is quite common in our subjects [35
], and we have not made attempts to specifically train the chimpanzees to produce only one of these behaviors within a given uptake period. Indeed it would be possible to train the chimpanzees to produce one, and only one (e.g., either a gesture or a vocalization, but not both), of these signals or even to produce only a single vocalization type. However, it is possible that this training might compromise the functional communicative relevance of these signals. Therefore, our aim was to capture the neurological correlates of these communicative behaviors in the chimpanzees and not necessarily the signal’s modality of production.
The total number of actions produced in the GV and BL tasks did differ among the subjects and between the tasks (see Table S1
). As described above (and in the Experimental Procedures), the chimpanzees in the GV and BL tasks were, more or less, self-paced. Therefore, the number and type of signals produced as well as their modality in the GV and BL tasks and the number of grasping responses in the BL task were not directly under the control of the experimenter during the uptake period. Our rationale for this procedure was to ensure that the subject’s motivation and arousal state did not differ significantly between the GV and BL tasks, enabling us to isolate neuronal metabolic activity related to the production of communicative signals. The number of communicative signals produced by all of the subjects in the GV task far exceeded those produced in the BL task (see Table S1
). Moreover, within the BL task, the number of reach and grasp responses produced by each subject far exceeded the number of communicative signals produced. In addition, the chimpanzee subjects did, in fact, produce various types of vocal signals in the GV condition, although the occurrence of attention-getting sounds in this condition far exceeded that of other vocalizations (Table S1
). Therefore, although it is not possible to distinguish the relative influence of the communicative modality (vocal or manual gesture) or the call type produced (attention-getting or other types of vocalizations) on the observed neuronal metabolic activity, consideration of the GV > BL tasks succeeded in isolating the communicative behaviors of the subjects relative to their manual motor actions.
Although these data indicate that the left IFG is involved in the production of communicative signals in chimpanzees, cytoarchitectonically, it is not clear what cell types fully comprise this region [36
]. Therefore, it is not possible to determine whether or not the neuronal metabolic activity reported in this study corresponds to an area within the chimpanzee IFG that contains Brodmann’s area 44/45 cells—those cells that comprise Broca’s area in humans. In fact, additional areas of significant activation are observed in the frontal orbital gyrus and the frontal pole (). Additional work is needed to explore the significance of these areas of activation. Notwithstanding, these data clearly implicate the left IFG and surrounding tissue within the prefrontal cortex and represent the first findings of the neural correlates associated with the production of communicative signals in chimpanzees.
Recently, it has been reported that the left IFG in humans is involved in both speech and American Sign Language production, suggesting that the functional role of this region is modality independent [12
]. The fact that during the production of their communicative signals, chimpanzees show significant activation in the left IFG in conjunction with other subcortical regions known to have strong connections to the prefrontal cortex [7
] suggests that the neurological substrates underlying language production in the human brain may have been present in the common ancestor of humans and chimpanzees.