Neuronal correlates of motion-defined shape perception in primate dorsal and ventral streams.

Human and non-human primates can readily perceive the shape of objects using visual motion. Classically, shape, and motion are considered to be separately processed via ventral and dorsal cortical pathways, respectively. However, many lines of anatomical and physiological evidence have indicated that these two pathways are likely to be interconnected at some stage. For motion-defined shape perception, these two pathways should interact with each other because the ventral pathway must utilize motion, which the dorsal pathway processes, to extract shape signal. However, it is unknown how interactions between cortical pathways are involved in neural mechanisms underlying motion-defined shape perception. We review evidence from psychophysical, lesion, neuroimaging and physiological research on motion-defined shape perception and then discuss the effects of behavioral demands on neural activity in ventral and dorsal cortical areas. Further, we discuss functions of two candidate sets of levels: early and higher-order cortical areas. The extrastriate area V4 and middle temporal (MT) area, which are reciprocally connected, at the early level are plausible areas for extracting the shape and/or constituent parts of shape from motion cues because neural dynamics are different from those during luminance-defined shape perception. On the other hand, among other higher-order visual areas, the anterior superior temporal sulcus likely contributes to the processing of cue-invariant shape recognition rather than cue-dependent shape processing. We suggest that sharing information about motion and shape between the early visual areas in the dorsal and ventral pathways is dependent on visual cues and behavioral requirements, indicating the interplay between the pathways.

Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain.

Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.

Color vision test for dichromatic and trichromatic macaque monkeys.

Dichromacy is a color vision defect in which one of the three cone photoreceptors is absent. Individuals with dichromacy are called dichromats (or sometimes "color-blind"), and their color discrimination performance has contributed significantly to our understanding of color vision. Macaque monkeys, which normally have trichromatic color vision that is nearly identical to humans, have been used extensively in neurophysiological studies of color vision. In the present study we employed two tests, a pseudoisochromatic color discrimination test and a monochromatic light detection test, to compare the color vision of genetically identified dichromatic macaques (Macaca fascicularis) with that of normal trichromatic macaques. In the color discrimination test, dichromats could not discriminate colors along the protanopic confusion line, though trichromats could. In the light detection test, the relative thresholds for longer wavelength light were higher in the dichromats than the trichromats, indicating dichromats to be less sensitive to longer wavelength light. Because the dichromatic macaque is very rare, the present study provides valuable new information on the color vision behavior of dichromatic macaques, which may be a useful animal model of human dichromacy. The behavioral tests used in the present study have been previously used to characterize the color behaviors of trichromatic as well as dichromatic new world monkeys. The present results show that comparative studies of color vision employing similar tests may be feasible to examine the difference in color behaviors between trichromatic and dichromatic individuals, although the genetic mechanisms of trichromacy/dichromacy is quite different between new world monkeys and macaques.

Gene conversion and purifying selection shape nucleotide variation in gibbon L/M opsin genes.

BACKGROUND: Routine trichromatic color vision is a characteristic feature of catarrhines (humans, apes and Old World monkeys). This is enabled by L and M opsin genes arrayed on the X chromosome and an autosomal S opsin gene. In non-human catarrhines, genetic variation affecting the color vision phenotype is reported to be absent or rare in both L and M opsin genes, despite the suggestion that gene conversion has homogenized the two genes. However, nucleotide variation of both introns and exons among catarrhines has only been examined in detail for the L opsin gene of humans and chimpanzees. In the present study, we examined the nucleotide variation of gibbon (Catarrhini, Hylobatidae) L and M opsin genes. Specifically, we focused on the 3.6~3.9-kb region that encompasses the centrally located exon 3 through exon 5, which encode the amino acid sites functional for the spectral tuning of the genes. RESULTS: Among 152 individuals representing three genera (Hylobates, Nomascus and Symphalangus), all had both L and M opsin genes and no L/M hybrid genes. Among 94 individuals subjected to the detailed DNA sequencing, the nucleotide divergence between L and M opsin genes in the exons was significantly higher than the divergence in introns in each species. The ratio of the inter-LM divergence to the intra-L/M polymorphism was significantly lower in the introns than that in synonymous sites. When we reconstructed the phylogenetic tree using the exon sequences, the L/M gene duplication was placed in the common ancestor of catarrhines, whereas when intron sequences were used, the gene duplications appeared multiple times in different species. Using the GENECONV program, we also detected that tracts of gene conversions between L and M opsin genes occurred mostly within the intron regions. CONCLUSIONS: These results indicate the historical accumulation of gene conversions between L and M opsin genes in the introns in gibbons. Our study provides further support for the homogenizing role of gene conversion between the L and M opsin genes and for the purifying selection against such homogenization in the central exons to maintain the spectral difference between L and M opsins in non-human catarrhines.

Feature to space conversion during target selection in the dorsolateral and ventrolateral prefrontal cortex of monkeys.

To investigate the neuronal mechanism of the process of selection of a target from an array of stimuli, we analysed neuronal activity of the lateral prefrontal cortex during the response period of a serial probe reproduction task. During the response period of this task, monkeys were trained to select a memorized target object from an array of three objects and make a saccadic eye movement toward it. Of 611 neurons, 74 neurons showed visual response and 56 neurons showed presaccadic activity during the response period. Among visual neurons, 27 showed array- and target-selectivity. All of these array- and target-selective visual responses were recorded from the ventrolateral prefrontal cortex (VLPFC). Among 56 neurons with presaccadic activity, nine showed target-selective activity, 17 showed target- and direction-selective activity, and 23 showed direction-selective activity. The target-selective, and the target- and direction-selective activities were recorded from the VLPFC, and the direction-selective activities were recorded from VLPFC and dorsolateral prefrontal cortex (DLPFC). The starting time of the activity was earlier for the target-selective, and target- and direction-selective activities in VLPFC, intermediate for the direction-selective activities in VLPFC, and later for the direction-selective activities in DLPFC. These results suggest that VLPFC plays a role in the process of selection of a target object from an array of stimuli, VLPFC and DLPFC play a role in determining the location of the target in space, and DLPFC plays a role in selecting a direction and making a decision to generate a saccadic eye movement.

Classification of extracellularly recorded neurons by their discharge patterns and their correlates with intracellularly identified neuronal types in the frontal cortex of behaving monkeys.

Neurons in the cerebral cortex are not homogeneous. However, neuronal types have been ignored in most previous work studying neuronal processes in behaving monkeys. We propose a new method to identify neuronal types in extracellular recording studies of behaving monkeys. We classified neurons as either bursting or non-bursting, and then classified the bursting neurons into three types: (i) neurons displaying a burst of many spikes (maximum number of spikes within a burst; NSB max > or = 8) at a high discharge rate (maximum interspike interval; ISI max < 5 ms); (ii) neurons displaying a burst of fewer spikes (NSB max < or = 5) at a high discharge rate (ISI max < 5 ms); and (iii) neurons displaying a burst of a few spikes (NSB max < or = 7) at relatively long ISIs (ISI max > 5 ms). We found that the discharge patterns of the four groups corresponded to those of regular spiking (RS), fast spiking (FS), fast rhythmic bursting (FRB) and intrinsic bursting (IB) neurons demonstrated in intracellular recording studies using in vitro slice preparations, respectively. In addition, we examined correlations with the task events for neurons recorded in the frontal eye field and neuronal interactions for pairs of neurons recorded simultaneously from a single electrode. We found that they were substantially different between RS and FS types. These results suggest that neurons in the frontal cortex of behaving monkeys can be classified into four types based on their discharge patterns, and that these four types contribute differentially to cortical operations.

Effect of fascial Manipulation® on reaction time.

INTRODUCTION: This study aimed to investigate the effects of fascial manipulation (FM) on muscle force and electrical activity. METHODS: Sixty healthy adult participants were randomly assigned to the FM intervention group (FM group; n = 20), static stretching intervention group (SS group; n = 20), and control group (C group; n = 20). The FM group underwent FM for the right brachial fascia (antecubitus) for 210 s. The SS group underwent static stretching of the right biceps brachii for 210 s. The C group was supine for 210 s. Participants were asked to flex the right elbow joint as quickly as possible after a light signal appeared during three sessions (before, immediately after, and 1 week after the intervention). During each session, the muscle activity of the right biceps brachii and bending force of the right elbow joint were measured. We calculated the reaction time (RT), pre-motor time (PMT), motor time (MT), time to peak force (TPF), and time to peak activity (TPA) from these measurements. RESULTS: The RT, MT, TPA, and TPF of the FM group were significantly shorter immediately after or 1 week after the intervention compared with those before the intervention. The RT, MT, TPA, and TPF of the FM group were significantly shorter than those of the SS group or C group immediately after or 1 week after the intervention. CONCLUSION: FM improved RT, MT, TPA, and TPA, and the effects lasted for 1 week. Both mechanical and neurological factors may contribute to improvements in motor performance after FM.

Color Perception in Protanomalous Female Macaca fascicularis.

Protanomalous females with X chromosome-linked color vision deficiency exhibit mild abnormalities, whereas dichromats show a distinct deficiency in discriminating certain color pairs. Dichromats have an advantage in detecting a textured target when it is camouflaged by red-green colors, owing to their insensitivity to these colors. However, it is not certain whether protanomalous females possess a similar advantage in breaking camouflage. Here, we introduce an animal model of dichromatic macaque monkeys and protanomalous females. We examined whether protanomalous females have the same advantage in breaking color camouflage as shown by dichromatic macaques. We also tested whether they could discriminate a certain color pair that trichromats could, where the dichromats are confused. Our experiments show that protanomalous macaques can break color camouflage, similar to dichromats, and can discriminate colors similarly to trichromats. Protanomalous females are thus thought to have the combined ecological advantages of being both trichromats and dichromats.

Modulation of V4 shifts from dependent to independent on feature during target selection.

We analyzed neuronal activities of visual area V4 of monkeys performing a delayed visual search task. To examine the temporal profile of factors influencing the neuronal activities, we conducted multiple regression analyses at 5 ms steps. During the period from 110 to 155 ms after the stimulus onset, there were neurons whose activity was suppressed when a target was presented near but beyond the neuron's receptive field (RF) compared to that when a target was within the RF. We referred this suppressive effect as an early period modulation. During the period from 155 to 280 ms after the stimulus onset, V4 activities were suppressed when a target was presented in any location outside of the neuron's RF. We referred this suppressive effect as a late period modulation. The magnitudes of the effect were equivalent across target locations when a target was beyond its RF. At the population level, while the modulation in the early period was correlated with stimulus selectivity, the modulation in the late period did not show such a correlation. These results suggest that V4 neurons have at least two distinct phases of modulations and those modulations contribute to select a target in the visual search task.

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.

Temporal property of single-cell activity in response to motion-defined shapes in monkey dorsal and ventral cortical areas.

In the primate brain, shape and motion are considered to be separately processed in the ventral and dorsal visual cortical areas, respectively. However, to achieve shape perception with a motion cue, shape and motion cannot be processed exclusively in separate cortical areas. Interactions between ventral and dorsal cortical areas are required, and yet, the neural mechanisms underlying motion-defined shape perception remain unclear. Here, we assessed the temporal properties of single-unit activity recorded from V4, the middle temporal area, and the anterior superior temporal sulcus while monkeys discriminated shapes defined by motion and luminance cues. Visual response latencies of V4 neurons were shorter in the luminance-cue condition than in the motion-cue condition. Meanwhile, the timings of initiation of shape selectivity were not different between cue conditions, indicating a difference in processing time. Middle temporal neurons were less shape modulated in the luminance-cue condition than in the motion-cue condition. Temporal properties of neural activities in the lower bank of anterior superior temporal sulcus were similar between cue conditions. These results suggest that an interaction of the ventral cortex with the dorsal cortex is required for shape discrimination with different visual cues.

Developmental trajectory of the corpus callosum from infancy to the juvenile stage: Comparative MRI between chimpanzees and humans.

How brains develop during early life is one of the most important topics in neuroscience because it underpins the neuronal functions that mature during this period. A comparison of the neurodevelopmental patterns among humans and nonhuman primates is essential to infer evolutional changes in neuroanatomy that account for higher-order brain functions, especially those specific to humans. The corpus callosum (CC) is the major white matter bundle that connects the cerebral hemispheres, and therefore, relates to a wide variety of neuronal functions. In humans, the CC area rapidly expands during infancy, followed by relatively slow changes. In chimpanzees, based on a cross-sectional study, slow changes in the CC area during the juvenile stage and later have also been reported. However, little is known about the developmental changes during infancy. A longitudinal study is also required to validate the previous cross-sectional observations about the chimpanzee CC. The present longitudinal study of magnetic resonance imaging scans demonstrates that the CC development in chimpanzees and humans is characterized by a rapid increase during infancy, followed by gradual increase during the juvenile stage. Several differences between the two species were also identified. First, there was a tendency toward a greater increase in the CC areas during infancy in humans. Second, there was a tendency toward a greater increase in the rostrum during the juvenile stage in chimpanzees. The rostral body is known to carry fibers between the bilateral prefrontal and premotor cortices, and is involved in behavior planning and control, verbal working memory, and number conception. The rostrum is known to carry fibers between the prefrontal cortices, and is involved in attention control. The interspecies differences in the developmental trajectories of the rostral body and the rostrum might be related to evolutional changes in the brain systems.

Elucidation of developmental patterns of marmoset corpus callosum through a comparative MRI in marmosets, chimpanzees, and humans.

The corpus callosum (CC) is present in all primate brains and is the major white matter tract connecting the cerebral hemispheres for integration of sensory, motor and higher-order cognitive information. The midsagittal area of the CC has frequently been used as a sensitive biomarker of brain development. Although the marmoset has been considered as an alternative non-human primate model for neuroscience research, the developmental patterns of the CC have not been explored. The present longitudinal study of magnetic resonance imaging demonstrated that marmosets show a rapid increase of CC during infancy, followed by a slow increase during the juvenile stage, as observed in chimpanzees and humans. Marmosets also show a tendency toward a greater increase in CC during late infancy and the juvenile stage, as observed in humans, but not in chimpanzees. However, several differences between marmosets and humans were identified. There was a tendency toward a greater maturation of the human CC during early infancy. Furthermore, there was a tendency toward a greater increase during late infancy and the juvenile stage in marmosets, compared to that observed in chimpanzees and humans. These differences in the developmental trajectories of the CC may be related to evolutional changes in social behavior.

Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in humans.

This study investigated whether 12 participants with color-vision deficiency had superior visual discrimination of color-camouflaged stimuli shown on a computer screen compared with 12 participants with normal trichromatic vision. Participants were asked to distinguish a circular pattern from other patterns in which textural elements differed from the background in orientation and thickness. In one condition, stimuli were single-colored, green or red; in the other condition, stimuli were color camouflaged with a green and red mosaic overlaid onto the pattern. Color-vision deficient participants selected the correct stimuli in the color-camouflaged condition as quickly as they did in the single-colored condition. However, normal color-vision participants took longer to select the correct choice in the color-camouflaged condition than in the single-colored condition. These results suggest that participants with color-vision deficiency may have a superior visual ability to discriminate the color-camouflaged stimuli.

Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys.

The concept that, after developmental periods, neocortical neurons become numerically stable and are normally nonrenewable has been challenged by a report of continuous neurogenesis in the association areas of the cerebral cortex in the adult Macaque monkey. Therefore, we have reexamined this issue in two different Macaque species using the thymidine analog bromodeoxyuridine (BrdU) as an indicator of DNA replication during cell division. We found several BrdU+/NeuN+ (neuronal nuclei) double-labeled cells, but cortical neurons, distinguished readily by their size and cytological and immunohistochemical properties, were not BrdU positive. We examined in detail the frontal cortex, where it is claimed that the largest daily addition of neurons has been made, but did not see migratory streams or any sign of addition of new neurons. Thus, we concluded that, in the normal condition, cortical neurons of adult primates, similar to other mammalian species, are neither supplemented nor renewable.

Correspondence of cue activity to reward activity in the macaque orbitofrontal cortex.

It has been reported that neurons in the orbitofrontal cortex (OFC) respond to emotionally significant events such as reward-predicting cues and/or the reward itself. The responses to reward-predicting cues are considered to carry the information of the predicted reward. However, few studies have focused on the relationship of the neuronal activity during a cue period with that during a reward period. We can infer that the cue responses of OFC neurons are correlated to the reward responses if they carry the information of the predicted reward. In this study, we focused on neurons that showed responses during both the cue and reward periods, and compared the response characteristics between these periods. We found 94 of 369 OFC neurons showed significant responses during both the cue and reward periods, and 43 of which preserved their selectivity between these periods. Furthermore, population analysis showed that stronger cue responses corresponded to stronger reward responses, and stronger reward responses corresponded to stronger cue responses. These results suggest that individual neurons in the OFC associate visual information with reward information, and contribute to the prediction of future rewards by forming reward representations.

Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses.

We determined the structures of long (L)-wavelength-sensitive and middle (M)-wavelength-sensitive opsin gene array of 58 male chimpanzees and we investigated relative sensitivity to red and green lights by electroretinogram flicker photometry. One subject had protanomalous color vision, while others had normal color vision. Unlike in humans, a polymorphic difference in the copy number of the genes and a polymorphic base substitution at amino acid position 180 were not frequently observed in chimpanzees.

Responses of monkey prefrontal neurons during the execution of transverse patterning.

Recent functional imaging studies have suggested that the prefrontal cortex (PF) is engaged in the performance of transverse patterning (TP), which consists of 3 conflicting discriminations (A+/B-, B+/C-, C+/A-). However, the roles of PF in TP are still unclear. To address this issue, we examined the neuronal responses in 3 regions [the principal sulcus (PS), dorsal convexity (DC), and medial prefrontal cortex (MPF)] of the macaque PF during the performance of an oculomotor version of TP. A delayed matching-to-sample (DMS) task was used as a control task. The TP task-responsive neurons were most abundant in MPF. We analyzed the dependency of each neuronal response on the task type (TP or DMS), target shape (A, B, or C), and target location (left or right). Immediately after the choice cue presentation, many MPF neurons showed task dependency. Interestingly, some of them already exhibited differential activity between the 2 tasks before the choice cue presentation. Immediately before the saccade, the number of target location-dependent neurons increased in MPF and PS. Among them, many MPF neurons were also influenced by the task type, whereas PS neurons tended to show location dependency without task dependency. These results suggest that MPF and PS are involved in the execution of TP: MPF appears to be more important in the target selection based on the TP rule, whereas PS is apparently more related to the response preparation. In addition, some neurons showed a postsaccadic response, which may be related to the feedback mechanism.

Neurons in the orbitofrontal cortex code both visual shapes and reward types.

It has been reported that neurons in the orbitofrontal cortex respond to visual cues that predict reward; however, few studies have focused on the neuronal correlates with the predicted reward type and the cue stimulus. In this study, we used a paired association task and introduced a reversal condition, in which cue stimuli that usually predict water were switched to predict juice, and vice versa. Of 111 cue-responsive neurons, 60 neurons (54.1%) depended on both the cue stimulus and the predicted reward type. The results suggest that neurons in the orbitofrontal cortex can code both visual and reward information, and contribute to the association between these two pieces of information according to the current combination of a cue stimulus and a reward type.

Variations in long- and middle-wavelength-sensitive opsin gene loci in crab-eating monkeys.

We analyzed variations in long (L)- and middle (M)-wavelength-sensitive opsin gene loci in crab-eating monkeys. Unlike humans, most monkeys have a single L and a single M gene. Two variant genotypes, one with only one opsin gene (dichromatic) and one with tandemly arrayed multiple genes, were also found in the monkeys. However, the frequency of the former was 0.47%, and that of the latter was 5% in the monkeys, while 2% and 66%, respectively, in Caucasian males. The two variants were found only in Java Island, Indonesia, and South Thailand, respectively. The data suggest that the frequency of each genotype is different among Old World primates.