The source-filter theory of whistle-like calls in marmosets: Acoustic analysis and simulation of helium-modulated voices.

Whistle-like high-pitched "phee" calls are often used as long-distance vocal advertisements by small-bodied marmosets and tamarins in the dense forests of South America. While the source-filter theory proposes that vibration of the vocal fold is modified independently from the resonance of the supralaryngeal vocal tract (SVT) in human speech, a source-filter coupling that constrains the vibration frequency to SVT resonance effectively produces loud tonal sounds in some musical instruments. Here, a combined approach of acoustic analyses and simulation with helium-modulated voices was used to show that phee calls are produced principally with the same mechanism as in human speech. The animal keeps the fundamental frequency (f0) close to the first formant (F1) of the SVT, to amplify f0. Although f0 and F1 are primarily independent, the degree of their tuning can be strengthened further by a flexible source-filter interaction, the variable strength of which depends upon the cross-sectional area of the laryngeal cavity. The results highlight the evolutionary antiquity and universality of the source-filter model in primates, but the study can also explore the diversification of vocal physiology, including source-filter interaction and its anatomical basis in non-human primates.

Monkeys perceive the orientation of objects relative to the vertical axis.

Orientation processing is essential for segmenting contour from the background, which allows perception of the shape and stability of objects. However, little is known about how monkeys determine the degree and direction of orientation. In this study, to determine the reference axis for orientation perception in monkeys, post-discrimination generalization tests were conducted following discrimination training between the 67.5° and 112.5° orientations and between the 22.5° and 157.5° orientations. After discrimination training between the 67.5° and 112.5° orientations, the slope of the generalization gradient around the S(+) orientation was broad, while the slope was steep after discrimination training between the 22.5° and 157.5° orientations. Comparing the shapes of the gradients indicated that the subjective distance between the 67.5° and 112.5° orientations was small, while the subjective distance between the 22.5° and 157.5° orientation was large. In other words, the monkeys recognized that the former and the latter distances were 45° and 135° across the vertical axis, rather than 135° and 45° across the horizontal axis, respectively. These findings indicate that the monkeys determined the degree and direction of the tilt using the vertical reference.

Common marmosets (Callithrix jacchus) cannot recognize global configurations of sound patterns but can recognize adjacent relations of sounds.

Processing the temporal configuration of discrete sounds to extract a regular pattern is fundamental to humans' faculties of perceiving words and musical phrases. To investigate such auditory pattern perception in monkeys, I trained two common marmosets to discriminate between AB-AB and AA-BB patterns under two training paradigms. One was an absolute discrimination task, in which the discrimination between these stimuli without reference cues was required. The other was a relative discrimination task, in which the detection of a change from one stimulus to the other was required. The marmosets failed in the absolute discrimination task but achieved the relative discrimination task. Failure in the absolute task indicated that the marmosets were unable to form a representation of the global sound patterns in their long-term memory stores. In contrast, success in the relative task indicated that the marmosets had short-term memory of ongoing sounds that enabled an online monitoring to detect deviations between incoming sounds and the anticipated upcoming sounds. Thus, the current findings imply that marmosets can at least perceive adjacent tone relations in an auditory stream regardless of the temporal configuration of the global sound patterns.

Auditory sequence perception in common marmosets (Callithrix jacchus).

One of the essential linguistic and musical faculties of humans is the ability to recognize the structure of sound configurations and to extract words and melodies from continuous sound sequences. However, monkeys' ability to process the temporal structure of sounds is controversial. Here, to investigate whether monkeys can analyze the temporal structure of auditory patterns, two common marmosets were trained to discriminate auditory patterns in three experiments. In Experiment 1, the marmosets were able to discriminate trains of either 0.5- or 2-kHz tones repeated in either 50- or 200-ms intervals. However, the marmosets were not able to discriminate ABAB from AABB patterns consisting of A (0.5-kHz/50-ms pulse) and B (2-kHz/200-ms pulse) elements in Experiment 2, and A (0.5-kHz/50-ms pulse) and B (0.5-kHz/200-ms pulse) [or A (0.5-kHz/200-ms pulse) and B (2-kHz/200-ms pulse)] in Experiment 3. Consequently, the results indicated that the marmosets could not perceive tonal structures in terms of the temporal configuration of discrete sounds, whereas they could recognize the acoustic features of the stimuli. The present findings were supported by cognitive and brain studies that indicated a limited ability to process sound sequences. However, more studies are needed to confirm the ability of auditory sequence perception in common marmosets.

Interaction between Perceived Action and Music Sequences in the Left Prefrontal Area.

Observing another person's piano play and listening to a melody interact with the observer's execution of piano play. This interaction is thought to occur because the execution of musical-action and the perception of both musical-action and musical-sound share a common representation in which the frontoparietal network is involved. However, it is unclear whether the perceptions of observed piano play and listened musical sound use a common neural resource. The present study used near-infrared spectroscopy to determine whether the interaction between the perception of musical-action and musical-sound sequences appear in the left prefrontal area. Measurements were obtained while participants watched videos that featured hands playing familiar melodies on a piano keyboard. Hand movements were paired with either a congruent or an incongruent melody. Two groups of participants (nine well-trained and nine less-trained) were instructed to identify the melody according to hand movements and to ignore the accompanying auditory track. Increased cortical activation was detected in the well-trained participants when hand movements were paired with incongruent melodies. Therefore, an interference effect was detected regarding the processing of action and sound sequences, indicating that musical-action sequences may be perceived with a representation that is also used for the perception of musical-sound sequences. However, in less-trained participants, such a contrast was not detected between conditions despite both groups featuring comparable key-touch reading abilities. Therefore, the current results imply that the left prefrontal area is involved in translating temporally structured sequences between domains. Additionally, expertise may be a crucial factor underlying this translation.

Intrinsic signal recording from a monkey whose behavior was maintained by a schedule of reinforcement.

Optical recording of cortical activity in awake monkeys has enhanced our understanding of the functional anatomy of the primary visual cortex (V1). However, cortical representation of visual cognition has not been studied by optical recording, even though the greatest merit of using awake animals is that they can offer advantages in studying cognitive function that anesthetized animals cannot. Thus far, the optical recording method has not been combined with tasks that accompany body movements because of concern about movement noise, although behavioral tasks are helpful in the study of animal cognition. Here, I tested the influence of body movements during the signal acquisition period on the resultant images. I recorded the intrinsic signals associating with different orientations from V1 of a monkey who was emitting behavior during the signal acquisition period. Although the monkey's behavior was maintained on a variable-interval schedule that typically induces a high rate of response, orientation maps were consistently obtained. Therefore, a successful recording under this operant regimen implies the applicability of the optical recording method to other behavioral tasks. Several constraints in applying optical recording to studies using behaving animals are also discussed.

Categorical perception of orientation in monkeys.

Structural and functional substrates of orientation processing in monkeys have been clarified. However, orientation perception in monkeys has not been fully studied. In this study, the cognitive mechanism that controls monkeys' perception of orientation was evaluated. After the monkeys were trained to discriminate between a cardinal and an oblique orientation (e.g., 0 degrees and 30 degrees), their perceptual mechanisms underlying orientation discrimination were tested by using six orientations, ranging from 0 degrees to 150 degrees, including ones used in the discrimination training. Generalization tests showed that the monkeys who were trained with cardinal orientations (e.g., 0 degrees) as positive stimuli generalized their responses to the other cardinal orientation (e.g., 90 degrees). Similarly, the monkeys who were trained with oblique orientations (e.g., 30 degrees) as positive stimuli generalized their responses to all other oblique orientations (e.g., 60 degrees, 120 degrees, and 150 degrees). These findings indicated that the monkeys abstracted the quality of the cardinal/oblique category from the physical features of orientation stimuli although they were not trained to do so. Such an abstraction also suggested a discrepancy between a continuously and orderly arranged cortical map and a discontinuously categorized perception of orientation. The present findings provide insight into the learning-correlated plasticity of cortical orientation preference.

Behavioral economic analysis of water intake in a laboratory rhesus macaque.

Behavioral economics is useful for understanding the influence of environmental manipulation on a variety of behaviors, including drug self-administration, food intake, and stock behavior. The present study employed behavioral economics to investigate the psychologically satisfying amount of water intake in a laboratory rhesus macaque. Our institutional guidelines set a minimum amount of daily water intake. However, no study to date has determined whether that minimum amount is psychologically sufficient. In the present experiment, a monkey lived in an individual cage in which the only water available was delivered by chain pulling. A fixed number of responses was required for water delivery. This fixed ratio (FR) of responses per water delivery was progressively increased from FR 2 to FR 10. The study findings showed that during the FR 2 condition, demand for water was saturated at 131.3 ml/kg body weight (BW) (ranging from 95.1 to 211.2). The monkey's daily intake of water decreased as FR size incrementally increased, approaching an asymptote under the FR 8 and FR 10 conditions. During the FR 8 and FR 10 conditions, responding ceased when this monkey earned 53.5 ml/kg-BW (ranging from 32.7 to 74.9) of water. Therefore, the amount of water obtained under these conditions might provide a psychologically satisfying amount. Although these values were obtained from the behavioral study of one monkey, they were almost equivalent to values in our institutional guidelines that were determined by veterinary observations. These findings imply that behavioral economics is useful for studying the welfare of laboratory animals.

Broca's area processes the hierarchical organization of observed action.

Broca's area has been suggested as the area responsible for the domain-general hierarchical processing of language and music. Although meaningful action shares a common hierarchical structure with language and music, the role of Broca's area in this domain remains controversial. To address the involvement of Broca's area in the processing action hierarchy, the activation of Broca's area was measured using near-infrared spectroscopy. Measurements were taken while participants watched silent movies that featured hand movements playing familiar and unfamiliar melodies. The unfamiliar melodies were reversed versions of the familiar melodies. Additionally, to investigate the effect of a motor experience on the activation of Broca's area, the participants were divided into well-trained and less-trained groups. The results showed that Broca's area in the well-trained participants demonstrated a significantly larger activation in response to the hand motion when an unfamiliar melody was played than when a familiar melody was played. However, Broca's area in the less-trained participants did not show a contrast between conditions despite identical abilities of the two participant groups to identify the melodies by watching key pressing actions. These results are consistent with previous findings that Broca's area exhibits increased activation in response to grammatically violated sentences and musically deviated chord progressions as well as the finding that this region does not represent the processing of grammatical structure in less-proficient foreign language speakers. Thus, the current study suggests that Broca's area represents action hierarchy and that sufficiently long motor training is necessary for it to become sensitive to motor syntax. Therefore, the notion that hierarchical processing in Broca's area is a common function shared between language and music may help to explain the role of Broca's area in action perception.

Effects of handedness and viewing perspective on Broca's area activity.

Given the fact that we understand observed action by a sensorimotor link that maps the action onto our motor representations, activity of the mirror neuron system may depend on the sensory and motor features of that action. To investigate this hypothesis, we recorded the activity of Broca's area (BCA) in right-handed individuals during observation of chopstick use using near-infrared spectroscopy. Individuals watched the right-handed or left-handed action recorded from the first-person's or third-person's perspective. Results show that the handedness of the observed action influences BCA activity, but the viewing perspective does not. We conclude that the motor aspect of the observed action is critical for BCA activation because this aspect is more relevant for simulating the observed action compared with the visuospatial aspect.

Measurement of neuronal activity in a macaque monkey in response to animate images using near-infrared spectroscopy.

Near-infrared spectroscopy (NIRS) has been used extensively for functional neuroimaging over the past decade, in part because it is considered a powerful tool for investigating brain function in human infants and young children, for whom other neuroimaging techniques are not suitable. In particular, several studies have measured hemodynamic responses in the occipital region in infants upon exposure to visual stimuli. In the present study, we used a multi-channel NIRS to measure neuronal activity in a macaque monkey who was trained to watch videos showing various circus animals performing acrobatic activities without fixing the head position of the monkey. Cortical activity from the occipital region was measured first by placing a probe comprising a 3 x 5 array of emitters and detectors (2 x 4 cm) on the area (area 17), and the robustness and stability of the results were confirmed across sessions. Cortical responses were then measured from the dorsofrontal region. The oxygenated hemoglobin signals increased in area 9 and decreased in area 8b in response to viewing the videos. The results suggest that these regions are involved in cognitive processing of visually presented stimuli. The monkey showed positive responsiveness to the stimuli from the affective standpoint, but its attentional response to them was an inhibitory one.

Orientation perception in rhesus monkeys (Macaca mulatta).

It was previously demonstrated that monkeys divide the orientation continuum into cardinal and oblique categories. However, it is still unclear how monkeys perceive within-category orientations. To better understand monkeys' perception of orientation, two experiments were conducted using five monkeys. In experiment 1, they were trained to identify either one cardinal or one oblique target orientation out of six orientations. The results showed that they readily identified the cardinal target whether it was oriented horizontally or vertically. However, a longer training period was needed to identify the oblique target orientation regardless of its degree and direction of tilt. In experiment 2, the same monkeys were trained to identify two-oblique target orientations out of six orientations. These orientations were paired, either sharing the degree of tilt, direction of tilt, or neither property. The results showed that the monkeys readily identified oblique orientations when they had either the same degree or direction of tilt. However, when the target orientations had neither the same degree nor direction of tilt, the animals had difficulty in identifying them. In summary, horizontal and vertical orientations are individually processed, indicating that monkeys do not have a category for cardinal orientation, but they may recognize cardinal orientations as non-obliques. In addition, monkeys efficiently abstract either the degree or the direction of tilt from oblique orientations, but they have difficulty combining these features to identify an oblique orientation. Thus, not all orientations within the oblique category are equally perceived.

Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque.

The ventral part of the third visual cortical complex, the ventral posterior area (VP) or V3v, is located between the ventral half of visual areas V2 and V4. Because of its location and the physiological properties of its neurons, VP has been considered to be involved in the ventral stream visual areas. The ventral stream visual areas such as V4 and TEO receive projections from the cytochrome oxidase (CO)-rich thin stripes and CO-poor interstripe regions of V2; however, which CO-modules project to VP remains unclear. Moreover, it is not clear whether V1 projects to VP. We injected retrograde tracers into VP and found that VP receives projections from V2 neurons not only in the CO-rich thin stripes and CO-poor interstripe regions but also in the CO-rich thick stripes. We also confirmed the virtual absence of inputs from V1 to VP. These results support the hypothesis that VP constitutes a distinct extrastriate visual area and also suggest that, in addition to color and shape information, VP may also process visual information related to space and disparity.

Chronic electrical stimulation of afferents from one eye changes ocular dominance of visual cortical neurons in kittens.

Binocular visual responsiveness of neurons in visual cortex of the cat can be changed by monocular visual deprivation in the critical period of postnatal development. It is hypothesized that afferents from each eye compete with one another for synaptic connections with cortical neurons so that less active afferents from the deprived eye fail to maintain the connections. This hypothesis predicts that an increase in inputs from one eye instead of decrease due to deprivation should also change binocular responsiveness of cortical neurons. However, the hypothesis has not successfully been tested with experimental activation of afferents from one eye. In the present study, we activated one of the optic nerves by chronic electrical stimulation of theta-burst type in behaving kittens for 2 days. After such a monocular activation, visual cortical neurons showed a significant ocular dominance shift in favor of the electrically activated eye, although neurons in the activated and nonactivated layers of the dorsal lateral geniculate nucleus had no biased visual responses. Also, we found no detectable difference between activated and nonactivated eye responses of cortical neurons in other response properties such as orientation selectivity. These results support the hypothesis that the balance between activities of both afferents is critical for formation or consolidation of each eye-specific pathway.