Akichika Mikami

Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain.

SINCE the anterior cingulate cortex (ACC) is known to be involved both in nociception and in anticipation that precedes the avoidance of aversive stimuli, the linking of these functions may be processed in the ACC. To test this hypothesis, we recorded single neuronal activities in the ACC of a macaque monkey while it was performing a pain-avoidance task and examined them with nociceptive cutaneous electric stimuli (ES). Thirty-six neurons responded in anticipation of the ES. Of these, 22 neurons were tested with the ES and 11 responded. These neurons could be those that are involved both in nociception and in pain anticipation that precedes the avoidance of noxious stimuli.

Directionally selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli.

SummaryBased on the fact that a great majority of cells in the middle temporal (MT) area of the macaque respond to movement of luminance contours with directional selectivity, this area has been thought to be concerned with the analysis of visual motion. However, objects can be discriminated from the background not only by differences in luminance but also by differences in color. It is possible that color signals are also used for motion analysis in MT. In the present study, we examined whether MT cells respond to movement of a pattern composed of pure color-contours. Using a color TV system, a moving color bar was displayed on a uniform background whose color was opponent with that of the bar. The main bar/background color combination we examined was magenta/cyan. Yellow/blue and cyan/ magenta combinations were also examined for some cells. The response of MT cells to movements of opponent-color stimuli was recorded while the bar/ background luminance ratio was changed from 1/10 to 10/1. In half of 89 cells tested in 3 monkeys, the response decreased considerably (disappeared completely in some cells) at a luminance ratio close to the human equiluminous condition. In the other half, a directional response persisted at any bar/background luminance ratio, though the response decreased to a varied extent (30–90% of the maximum response) near the ratio 1 (human equiluminous condition). The average magnitude of the equiluminous response to the magenta/cyan stimulus for the overall population was about 35% of the maximal response when the length of the bar (0.5° in width) and the movement amplitude were set to be optimal for individual cells, i.e. smaller than 15° and 10° of visual angle, respectively. This fall to 23% when the bar length and movement amplitude were limited to 2°. The same cell responded to pure color-contours of yellow/ blue as well as of cyan/magenta combinations. Thus, MT can detect the direction of movement of pure color-contours, although the sensitivity is less than for luminance contours.

Inferotemporal neuron activities and color discrimination with delay

Abstract Neuron activity was recorded from the inferotemporal cortex (IT)of rhesus monkeys while they were performing a visual color discrimination task, in which a light (green or red) was illuminated twice with a delay period of 1–5 sec. Two kinds of task were employed. The first was a visual short-term memory task, originally described by Konorski (task I), and the second was its slightly modified version (task II). If the first stimulus (sample) and the second (matching) were the same in color, the monkey pressed one of two levers and if two stimuli were different, the monkey pressed the other. In task I, the matching stimulus signaled ‘GO’ for lever press. In task II, after visual stimuli, another delay period and then auditory stimulus, indicating ‘GO’ for lever press, were added. Out of 101 task related neurons, 57 were recorded during task I and 44 were during task II. Most of these were activated by visual stimuli and these were divided into two classes: ones responding non-differentially to different colors (45 neurons) and the other responding differentially to different colors (37 neurons). In task I, 8 neurons showed increases only after matching stimuli and one increased only after sample stimuli. Out of 33 neurons activated by both stimuli, 20 showed stronger responses to matching stimuli and others showed increase or decrease of equal degree. Out of task II-related neurons, 40 were activated visually during sample and matching periods and 20 showed stronger responses to matching stimuli. It is said that in these task visually activated neurons tended to show stronger responses to matching than to sample stimuli. Activity related to the lever press was not found. It was suggested from these results that the IT neurons were related to a process of visual discrimination, so that a physically identical stimulus which had a different meaning in the behavioral context would be differentiated.

Anterior cingulate activity during pain-avoidance and reward tasks in monkeys.

We recorded single neuronal activities in the anterior cingulate cortex of monkeys while they were performing discriminative pain-avoidance and reward tasks: a prediction cue was presented for 0.5-1.5 s, followed by a red or green discrimination cue (1:1, random) for 1.0 s; painful stimuli were presented if the monkey failed to respond during the red cue; a reward was given, subsequent to a cued 1 s delay, if the monkey responded after the green cue. Among 775 neurons recorded, 196 neurons showed significant activity during one or more observation periods; 36 during the prediction period; 77 during the discrimination period; 41 during the delay period; 85 during the response period; 40 during the pre-reward period; and 15 during the reward-ingestion period. Of 77 neurons activated during the discrimination period, 47 showed exclusive activity either during the red (34) or during the green (13) cue: of 85 neurons activated during the response period, 64 showed exclusive activity either for pain-avoidance (37) or obtaining a reward (27). Control experiments confirmed that the neuronal activity could not be attributed to simple visual or motor processes. The results suggest that some anterior cingulate neurons are involved with anticipation of, and response selection for, imminent events.

Descent of the larynx in chimpanzee infants

The human larynx descends during infancy and the early juvenile periods, and this greatly contributes to the morphological foundations of speech development. This developmental phenomenon is believed to be unique to humans. This concept has formed a basis for paleoanthropological studies on the origin and evolution of human speech. We used magnetic resonance imaging to study the development of three living chimpanzees and found that their larynges also descend during infancy, as in human infants. This descent was completed primarily through the rapid descent of the laryngeal skeleton relative to the hyoid, but it was not accompanied by the descent of the hyoid itself. The descent is possibly associated with developmental changes of the swallowing mechanism. Moreover, it contributes physically to an increased independence between the processes of phonation and articulation for vocalization. Thus, the descent of the larynx and the morphological foundations for speech production must have evolved in part during hominoid evolution, and not in a single shift during hominid evolution.

Neurons in the macaque orbitofrontal cortex code relative preference of both rewarding and aversive outcomes.

Many studies have shown that the orbitofrontal cortex (OFC) is involved in the processing of emotional information. However, although some lines of study showed that the OFC is also involved in negative emotions, few electrophysiological studies have focused on the characteristics of OFC neuronal responses to aversive information at the individual neuron level. On the other hand, a previous study has shown that many OFC neurons code relative preference of available rewards. In this study, we aimed to elucidate how reward information and aversive information are coded in the OFC at the individual neuron level. To achieve this aim, we introduced the electrical stimulus (ES) as an aversive stimulus, and compared the neuronal responses to the ES-predicting stimulus with those to reward-predicting stimuli. We found that many OFC neurons showed responses to both the ES-predicting stimulus and the reward-predicting stimulus, and they code relative preference of not only the reward outcome but also the aversive outcome. This result suggests that the same group of OFC neurons code both reward and aversive information in the form of relative preference.

Oscillatory neuronal activity related to visual short-term memory in monkey temporal pole

The activity of single neurons was recorded extracellularly from the temporal pole of monkeys while they were performing a visual short-term memory task. Neurons in the ventral part of the temporal pole showed sustained firing during the memorization delay period of the task when the monkey was remembering particular visual stimuli. The presence and absence of the firing were correlated with the correct and incorrect performance of the task, respectively. The sustained firing showed oscillation. The data suggest that visual information was stored as sustained firing among certain group of neurons producing oscillations.

Neuronal activity in the frontal eye field of the monkey is modulated while attention is focused on to a stimulus in the peripheral visual field, irrespective of eye movement

We tested the hypothesis that the frontal eye field (FEF) is involved in attention to the peripheral visual field (PVF). Neuronal activity was recorded in the FEF of two monkeys while they were performing three oculomotor tasks. In the visual attention task (VAT), the monkeys released a lever when a test stimulus (TS) presented in the PVF dimmed while they were looking at a central fixation point (FP). In the visual saccade task (VST), the monkeys exhibited saccadic eye movements when the FP was extinguished. In the visual fixation task (VFT), the monkeys released the lever when the FP dimmed. Overall, the activities of 80 FEF neurons were examined. The responses to visual stimuli of 41 of these neurons (51%) were modulated during the VAT. Twenty-five neurons showed pre-saccadic activity. Of these, 13 neurons (52%) exhibited activity modulation during the VAT. Eighteen neurons showed no pre-saccadic activity. Of these, 10 neurons (56%) exhibited activity modulation during the VAT. These results suggest that the FEF is involved in selecting the visual stimuli relevant to performing a task irrespective of eye movements.

During pain-avoidance neurons activated in the macaque anterior cingulate and caudate

Lesions in either the anterior cingulate cortex (ACC) or the caudate nucleus (CN) impair avoidance behavior from noxious somatic stimuli, so these two areas may play a similar role in pain-avoidance behavior. To test this hypothesis, we recorded single neuronal activities in the ACC and in the CN of a monkey while it was performing a pain-avoidance task. Ten of 136 ACC and eleven of 160 CN neurons responded selectively during pain-avoidance behavior. We found little difference in the population distribution or in the response latency and duration. Our present findings are in accordance with previous lesion and anatomical studies which suggest that these two regions could function as one module in pain-avoidance behavior.

Vision: Dichromatism in macaque monkeys

Old World primates have trichromatic vision because they have three types of cone photoreceptor, each of which is maximally sensitive to short, middle or long wavelengths of light. Although a proportion of human males (about 8% of caucasians, for example) have X-chromosome-linked colour-vision abnormalities, no non-human Old World primates have been found to be colour-vision defective. We have tested 3,153 macaque monkeys but found only three dichromats, a frequency that is much lower than in humans.