Auditory ERPs to Stimulus Deviance in an Awake Chimpanzee (Pan troglodytes): Towards Hominid Cognitive Neurosciences

BACKGROUND: For decades, the chimpanzee, phylogenetically closest to humans, has been analyzed intensively in comparative cognitive studies. Other than the accumulation of behavioral data, the neural basis for cognitive processing in the chimpanzee remains to be clarified. To increase our knowledge on the evolutionary and neural basis of human cognition, comparative neurophysiological studies exploring endogenous neural activities in the awake state are needed. However, to date, such studies have rarely been reported in non-human hominid species, due to the practical difficulties in conducting non-invasive measurements on awake individuals. METHODOLOGY/PRINCIPAL FINDINGS: We measured auditory event-related potentials (ERPs) of a fully awake chimpanzee, with reference to a well-documented component of human studies, namely mismatch negativity (MMN). In response to infrequent, deviant tones that were delivered in a uniform sound stream, a comparable ERP component could be detected as negative deflections in early latencies. CONCLUSIONS/SIGNIFICANCE: The present study reports the MMN-like component in a chimpanzee for the first time. In human studies, various ERP components, including MMN, are well-documented indicators of cognitive and neural processing. The results of the present study validate the use of non-invasive ERP measurements for studies on cognitive and neural processing in chimpanzees, and open the way for future studies comparing endogenous neural activities between humans and chimpanzees. This signifies an essential step in hominid cognitive neurosciences

Neural Correlates of Face and Object Perception in an Awake Chimpanzee (Pan Troglodytes) Examined by Scalp-Surface Event-Related Potentials

BACKGROUND: The neural system of our closest living relative, the chimpanzee, is a topic of increasing research interest. However, electrophysiological examinations of neural activity during visual processing in awake chimpanzees are currently lacking. METHODOLOGY/PRINCIPAL FINDINGS: In the present report, skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of faces and objects in two experiments. In Experiment 1, human faces and stimuli composed of scrambled face images were displayed. In Experiment 2, three types of pictures (faces, flowers, and cars) were presented. The waveforms evoked by face stimuli were distinguished from other stimulus types, as reflected by an enhanced early positivity appearing before 200 ms post stimulus, and an enhanced late negativity after 200 ms, around posterior and occipito-temporal sites. Face-sensitive activity was clearly observed in both experiments. However, in contrast to the robustly observed face-evoked N170 component in humans, we found that faces did not elicit a peak in the latency range of 150-200 ms in either experiment. CONCLUSIONS/SIGNIFICANCE: Although this pilot study examined a single subject and requires further examination, the observed scalp voltage patterns suggest that selective processing of faces in the chimpanzee brain can be detected by recording surface ERPs. In addition, this non-invasive method for examining an awake chimpanzee can be used to extend our knowledge of the characteristics of visual cognition in other primate species

Brain response to affective pictures in the chimpanzee.

チンパンジーも他者の表情を素早く察知 -脳波測定による解明-.京都大学プレスリリース. 2013-02-26.Advancement of non-invasive brain imaging techniques has allowed us to examine details of neural activities involved in affective processing in humans; however, no comparative data are available for chimpanzees, the closest living relatives of humans. In the present study, we measured event-related brain potentials in a fully awake adult chimpanzee as she looked at affective and neutral pictures. The results revealed a differential brain potential appearing 210 ms after presentation of an affective picture, a pattern similar to that in humans. This suggests that at least a part of the affective process is similar between humans and chimpanzees. The results have implications for the evolutionary foundations of emotional phenomena, such as emotional contagion and empathy

Fetal brain development in chimpanzees versus humans.

世界で初めてチンパンジー胎児の脳成長が明らかに : ヒトの脳の巨大化はすでに胎児期からスタート. 京都大学プレスリリース. 2012-09-25.It is argued that the extraordinary brain enlargement observed in humans is due to not only the human-specific pattern of postnatal brain development, but also to that of prenatal brain development [1, 2]. However, the prenatal trajectory of brain development has not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, we tracked fetal development of the chimpanzee brain from approximately 14 to 34 weeks of gestation (just before birth) in utero using three-dimensional ultrasound imaging. The results were compared with those obtained for the human brain during approximately the same period. We found that the brain volume of chimpanzee fetuses was only half that of human fetuses at 16 weeks of gestation. Moreover, although the growth velocity of brain volume increased until approximately 22 weeks of gestation in both chimpanzees and humans, chimpanzee fetuses did not show the same accelerated increase in brain volume as human fetuses after that time. This suggests that maintenance of fast development of the human brain during intrauterine life has contributed to the remarkable brain enlargement observed in humans

Neural representation of face familiarity in an awake chimpanzee

Evaluating the familiarity of faces is critical for social animals as it is the basis of individual recognition. In the present study, we examined how face familiarity is reflected in neural activities in our closest living relative, the chimpanzee. Skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of familiar and unfamiliar chimpanzee faces (Experiment 1) and human faces (Experiment 2). The ERPs evoked by chimpanzee faces differentiated unfamiliar individuals from familiar ones around midline areas centered on vertex sites at approximately 200 ms after the stimulus onset. In addition, the ERP response to the image of the subject’s own face did not significantly diverge from those evoked by familiar chimpanzees, suggesting that the subject’s brain at a minimum remembered the image of her own face. The ERPs evoked by human faces were not influenced by the familiarity of target individuals. These results indicate that chimpanzee neural representations are more sensitive to the familiarity of conspecific than allospecific faces

Brain activity in an awake chimpanzee in response to the sound of her own name

The brain activity of a fully awake chimpanzee being presented with her name was investigated. Event-related potentials (ERPs) were measured for each of the following auditory stimuli: the vocal sound of the subject's own name (SON), the vocal sound of a familiar name of another group member, the vocal sound of an unfamiliar name and a non-vocal sound. Some differences in ERP waveforms were detected between kinds of stimuli at latencies at which P3 and Nc components are typically observed in humans. Following stimulus onset, an Nc-like negative shift at approximately 500 ms latency was observed, particularly in response to SON. Such specific ERP patterns suggest that the chimpanzee processes her name differently from other sounds

Combination of stimulus tones for each condition.

<p>Combination of stimulus tones for each condition.</p

Mean amplitudes (<i>SD</i>) of standard- and deviant-waves for each condition and scalp position.

<p><i>Note</i>. Mean amplitudes are indicated with <i>SD</i> values in parenthesis. std: values for standard stimuli; dev: values for deviant stimuli.</p