Feature-based attention modulates orientation-selective responses in human visual cortex

How does feature-based attention modulate neural responses? We used adaptation to quantify the effect of feature-based attention on orientation-selective responses in human visual cortex. Observers were adapted to two superimposed oblique gratings while attending to one grating only. We measured the magnitude of attention-induced orientation-selective adaptation both psychophysically, by the behavioral tilt aftereffect, and physiologically, using fMRI response adaptation. We found evidence for orientation-selective attentional modulation of neuronal responses-a lower fMRI response for the attended than the unattended orientation-in multiple visual areas, and a significant correlation between the magnitude of the tilt aftereffect and that of fMRI response adaptation in V1, the earliest site of orientation coding. These results show that feature-based attention can selectively increase the response of neuronal subpopulations that prefer the attended feature, even when the attended and unattended features are coded in the same visual areas and share the same retinotopic location.     

Distribution of attention modulates salience signals in early visual cortex

Previous research has shown that the extent to which people spread attention across the visual field plays a crucial role in visual selection and the occurrence of bottom-up driven attentional capture. Consistent with previous findings, we show that when attention was diffusely distributed across the visual field while searching for a shape singleton, an irrelevant salient color singleton captured attention. However, while using the very same displays and task, no capture was observed when observers initially focused their attention at the center of the display. Using event-related fMRI, we examined the modulation of retinotopic activity related to attentional capture in early visual areas. Because the sensory display characteristics were identical in both conditions, we were able to isolate the brain activity associated with exogenous attentional capture. The results show that spreading of attention leads to increased bottom-up exogenous capture and increased activity in visual area V3 but not in V2 and V1.     

Dissociable modulation of overt visual attention in valence and arousal revealed by topology of scan path

Emotional stimuli have evolutionary significance for the survival of organisms; therefore, they are attention-grabbing and are processed preferentially. The neural underpinnings of two principle emotional dimensions in affective space, valence (degree of pleasantness) and arousal (intensity of evoked emotion), have been shown to be dissociable in the olfactory, gustatory and memory systems. However, the separable roles of valence and arousal in scene perception are poorly understood. In this study, we asked how these two emotional dimensions modulate overt visual attention. Twenty-two healthy volunteers freely viewed images from the International Affective Picture System (IAPS) that were graded for affective levels of valence and arousal (high, medium, and low). Subjects' heads were immobilized and eye movements were recorded by camera to track overt shifts of visual attention. Algebraic graph-based approaches were introduced to model scan paths as weighted undirected path graphs, generating global topology metrics that characterize the algebraic connectivity of scan paths. Our data suggest that human subjects show different scanning patterns to stimuli with different affective ratings. Valence salient stimuli (with neutral arousal) elicited faster and larger shifts of attention, while arousal salient stimuli (with neutral valence) elicited local scanning, dense attention allocation and deep processing. Furthermore, our model revealed that the modulatory effect of valence was linearly related to the valence level, whereas the relation between the modulatory effect and the level of arousal was nonlinear. Hence, visual attention seems to be modulated by mechanisms that are separate for valence and arousal.     

Rhesus macaques (Macaca mulatta) are not neophobic toward novel food with a high sugar content

While we know that food neophobia in nonhuman primates is affected by social factors, little is known about how palatability, and specifically sugar content, might ameliorate a monkey's hesitancy to eat a novel food. It is likely that an innate preference for sweet substances would alter an animal's typical neophobic response. To test this, I presented nine male rhesus macaques with novel foods that contained a low, high, or no amount of sugar. As expected, the monkeys exhibited a neophobic response to the no-sugar novel foods but not to the high-sugar novel foods. Previous research on food neophobia may need to be reevaluated in light of the effects of sugar content on the neophobic response.     

Collective arousal when reuniting after temporary separation in Tonkean macaques

Celebrations and bursts of communal joy can occur spontaneously in human communities based on mechanisms of emotional contagion. Some examples of similar collective excitement have been reported in animals when they reunite or anticipate rewards, but little is known about the processes and meaning of these multiple interactions. We experimentally studied such collective arousals in two captive groups of Tonkean macaques (Macaca tonkeana) within the context of reunions following the temporary separation of two subgroups. We compared the behaviors of individuals after separation periods of 2 and 48 h with a control period with no separation. This study showed that it is possible to reproducibly induce bursts of friendly interactions in which groupmates run around over a period of several minutes, embracing and grasping one another while displaying numerous affiliative vocalizations and facial expressions. The longer the period of separation, the higher and longer-lasting the rates of affiliative interactions were. Individuals affiliated more frequently with groupmates from a previously separated subgroup than with those having stayed in their own subgroup. Collective arousal was followed by a quieter period characterized by high rates of contact-sitting and social grooming. These results point at the role of collective arousals in social cohesion; they could resolve social tension and renew social relationships. We propose that the emotional state experienced by Tonkean macaques during such events represents a disposition similar to that giving rise to what we humans call "shared joy."     

Persistent sympathetic nervous system arousal associated with tethering in cynomolgus macaques

The swivel-tether system has been used extensively in biomedical research involving nonhuman primates, yet there has been little or no investigation into potential adverse influences of this form of restraint on research results. In the study described here, a portable electrocardiographic telemetry system was used for continuous monitoring of the heart rate of 26 cynomolgus monkeys while: (a) pair-caged, 8 weeks prior to tethering; (b) singly-caged, tethered; (c) singly-caged, tethered, administered propranolol (30 mg/kg/day) in the diet; (d) group-housed (five monkeys per group), 1 week after group formation; and (e) group-housed (five monkeys per group), 4 weeks after group formation. Tethering resulted in persistent elevations in heart rate relative to the other conditions. Administration of propranolol, a beta-adrenergic antagonist, resulted in an abrupt, sustained decrease in heart rate indicating that the increase in heart rate associated with tethering was due to persistent stimulation of the sympathetic nervous system. Since multiple aspects of cardiovascular function are influenced by the sympathetic nervous system, and other organs and systems (e.g., pituitary-gonadal) also may be affected, investigators using the swivel-tether system should be cognizant of these potential effects when designing experiments and interpreting the results.     

Social behavior in aged rhesus macaques

This study investigated the relationship between chronological age and social behavior in 42 adult male and female rhesus macaques (Macaca mulatta) in three specific areas: social interactions, social roles, and social networks. While both old males and old females share behavioral differences associated with senescence, this study reports that old females and old males are distinct in their social behaviors, both from each other and from other adults. Many of these differences appear progressive across age classes, e.g., declining across age classes in females and increasing across age classes in males. Old females are less social and have smaller social networks than other females, while the opposite was found to be true of old males. An explanation for the sex-based differences in aged social behavior and social networks reported in this study may originate in rhesus matrifocal social structure.     

Evidence that emotion mediates social attention in rhesus macaques

Background

Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual’s emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.

Methodology

We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.

Principle Findings

The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.

Conclusions/Significance

These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.     

Rhesus macaques compensate for reproductive delay following ecological adversity early in life

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and life span. However, long‐lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter life spans. Here, we quantify the effects of major hurricanes and density dependence as sources of early‐life ecological adversity on Cayo Santiago rhesus macaque female reproduction and decompose their effects onto the mean age‐specific fertility, reproductive pace, and lifetime reproductive success (LRS). Females experiencing major hurricanes exhibit a delayed reproductive debut but maintain the pace of reproduction past debut and show a higher mean fertility during prime reproductive ages, relative to unaffected females. Increasing density at birth is associated to a decrease in mean fertility and reproductive pace, but such association is absent at intermediate densities. When combined, our study reveals that hurricanes early in life predict a delay‐overshoot pattern in mean age‐specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, this long‐lived population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no major negative fitness outcomes. Density presents a more complex relation with reproduction that suggests females experiencing a population regulated at intermediate densities early in life will escape density dependence and show optimized reproductive schedules. Our results support hypotheses about life history trade‐offs in which adversity‐affected females ensure their future reproductive potential by allocating more energy to growth or maintenance processes at younger adult ages.     

Rhesus rhadinovirus infection in healthy and SIV-infected macaques at Tulane National Primate Research Center

Rhesus rhadinovirus (RRV) infection was quantified in peripheral blood mononuclear cells (PBMC) from healthy and simian immunodeficiency virus (SIV)-infected rhesus macaques (Macaca mulatta) at the Tulane National Primate Research Center and in a large collection of simian acquired immunodeficiency syndrome--(SAIDS)-associated lymphomas. Quantification of RRV load was performed by real-time PCR using amplification primers specific for the RRV interleukin-6 homologue (RRV vIL-6). RRV infection was detected infrequently and at low levels in PBMC of randomly selected healthy animals. Examination of longitudinally collected PBMC from 22 SIV-infected animals throughout progression to SAIDS revealed similarly low RRV loads that sometimes increased with advancing disease. RRV infection was detected more frequently in the peripheral blood of SIV-infected animals than in healthy animals. Examination of SAIDS-associated lymphomas showed that RRV is rare within the tumor mass, likely representing infection in an occasional tumor-infiltrating cell or contaminating blood. The results indicate that RRV infection in PBMC is not predictive of, and is apparently not required for, development of lymphoma or hyperplastic lymphadenopathy in SIV-infected animals at TNPRC.     

Social odours, sexual arousal and pairbonding in primates

We describe the role of social odours in sexual arousal and maintaining pairbonds in biparental and cooperatively breeding primates. Social odours are complex chemical mixtures produced by an organism that can simultaneously provide information about species, kinship, sex, individuality and reproductive state. They are long lasting and have advantages over other modalities. Both sexes are sensitive to changes in odours over the reproductive cycle and experimental disruption of signals can lead to altered sexual behaviour within a pair. We demonstrate, using functional magnetic resonance imaging (fMRI), that social odours indicating reproductive state directly influence the brain areas responsible for sexual behaviour. Social odours also influence other brain areas typically involved in motivation, memory and decision making, suggesting that these signals have more complex functions in primates than mere sexual arousal. We demonstrate a rapid link between social odours and neuroendocrine responses that are modulated by a male's social status. Recent work on humans shows similar responses to social odours. We conclude with an integration of the importance of social odours on sexual arousal and maintaining pairbonds in socially biparental and cooperatively breeding species, suggesting new research directions to integrate social behaviour, neural activation and neuroendocrine responses.     

Social behaviour of stump-tailed macaques in captivity

Facial expressions and gestures seen in eight wild caught adult and three laboratory born stump-tailed macaques are described. Systematic observations, designed to show the association of these with attack, fleeing, grooming, or copulating are reported. The behaviour is in general very similar to that of other macaques.However, we find that Presenting and Lipsmacking are given by animals who are likely to win or lose fights and are shown to babies. These are clearly not just appeasing in function (reducing attack) but also reassuring (reducing fleeing). Two forms of non-sexual Presenting were found to follow and lead to different behaviour. Copulation appears to be different from that described in rhesus, ejaculation occuring on each mounting, which last for around one minute. In our animals the males bit the females during the later stages of copulation, but seldom showed any signs of aggression when not mounting.Grin-lipsmacking (lipsmacking with lips retracted exposing the teeth) is associated with fleeing, with changing from fighting to grooming and with copulation. A link between these situations may be provided earlier in development by the observation that mothers comfort frightened, Grin-lipsmacking babies by manipulating the external genitalia.     

Calmodulin differentially modulates Smad1 and Smad2 signaling

The members of the Smad protein family are intracellular mediators of transforming growth factor beta (TGF-beta) signaling. Smad1 transduces bone morphogenetic protein signals, inducing formation of ventral mesoderm in Xenopus embryos, whereas Smad2 transduces activin/TGF-beta signals, generating dorsal mesoderm. Calmodulin directly binds to many Smads and was shown to down-regulate Smad2 activity in a cell culture system (Zimmerman, C. M., Kariapper, M. S. T., and Mathews, L. S. (1997) J. Biol. Chem. 273, 677-680). Here, we extend those data and demonstrate that calmodulin alters Smad signaling in living embryos, increasing Smad1 activity while inhibiting Smad2 function. To characterize this regulation, we undertook a structure-function analysis and found that calmodulin binds to two distinct and conserved regions in both Smad1 and Smad2. Receptor tyrosine kinase signaling also modifies Smad activity (Kretzschmar, M., Doody, J., and Massagué, J. (1997) Nature 389, 618-622; Kretzschmar, M., Doody, J., Timokhina, I., and Massagué, J. (1999) Genes Dev. 13, 804-816; de Caestecker, M. P., Parks, W. T., Frank, C. J., Castagnino, P., Bottaro, D. P., Roberts, A. B., and Lechleider, R. J. (1998) Genes Dev. 12, 1587-1592). We show that calmodulin binding to Smads inhibits subsequent Erk2-dependent phosphorylation of Smads and vice versa. These observations suggest the presence of a cross-talk between three major signaling cascades as follows: Ca(2+)/calmodulin, receptor tyrosine kinase, and TGF-beta pathways.     

Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner

Tissue transglutaminase is a unique member of the transglutaminase family as it not only catalyzes a transamidating reaction, but also binds and hydrolyzes GTP and ATP. Tissue transglutaminase has been reported to be pro-apoptotic, however, conclusive evidence is still lacking. To elucidate the role of tissue transglutaminase in the apoptotic process human neuroblastoma SH-SY5Y cells were stably transfected with vector only (SH/pcDNA), wild-type tissue transglutaminase (SH/tTG) and tissue transglutaminase that has no transamidating activity but retains its other functions (SH/C277S). In these studies three different apoptotic stimuli were used osmotic stress, staurosporine treatment and heat shock to delineate the role of tissue transglutaminase as a transamidating enzyme in the apoptotic process. In SH/tTG cells, osmotic stress and staurosporine treatments resulted in significantly greater caspase-3 activation and apoptotic nuclear changes then in SH/pcDNA or SH/C277S cells. This potentiation of apoptosis in SH/tTG cells was concomitant with a significant increase in the in situ transamidating activity of tissue transglutaminase. However, in the heat shock paradigm, which did not result in any increase in the transamidating activity in SH/tTG cells, there was a significant attenuation of caspase-3 activity, LDH release and apoptotic chromatin condensation in SH/tTG and SH/C277S cells compared with SH/pcDNA cells. These findings indicate for the first time that the effect of tissue transglutaminase on the apoptotic process is highly dependent on the type of the stimuli and how the transamidating activity of the enzyme is affected. Tissue transglutaminase facilitates apoptosis in response to stressors that result in an increase in the transamidating activity of the enzyme. However, when the stressors do not result in an increase in the transamidating activity of tissue transglutaminase, than tissue transglutaminase can ameliorate the apoptotic response through a mechanism that is independent of its transamidating function. Further, neither the phosphatidylinositol-3-kinase pathway nor the extracellular-regulated kinase pathway is downstream of the modulatory effects of wild-type tissue transglutaminase or C277S-tissue transglutaminase in the apoptotic cascade.     

Social housing and pregnancy outcome in captive pigtailed macaques

We present a retrospective analysis of 30 years of breeding records from a colony of pigtailed macaques at the University of Washington's Regional Primate Research Center, specifically examining the effects on pregnancy outcome of sire presence, presence of other pregnant females, group stability, overall group size, and dam age and parity. Data on 2,040 pregnancies (1,890 live births) of socially housed pigtailed macaques (Macaca nemestrina) were obtained from the Washington Regional Primate Research Center's animal colony records from 1967 to 1996. Our results suggest that the presence of the sire and other pregnant females, fewer moves, and lower parity increases the probability of a viable birth. In viable and nonviable births, gestation length was positively related to contact with the sire and other pregnant females, number of moves, and dam age. Once the effect of gestational age was taken into account, birthweight increased with increasing parity and decreased with dam age. Clinical treatment of the dam decreased as sire presence and group size increased and number of moves decreased. The length of treatment was dependent on the number of moves experienced by the dam, with more moves associated with longer treatments. Sire presence was the single most important factor in nearly all measures of reproductive outcome. Am. J. Primatol. 47:153–163, 1999. © 1999 Wiley‐Liss, Inc.     

Social and nonsocial stimuli and juvenile hormone titer in a male burying beetle, Nicrophorus orbicollis

We investigated the interaction of social and nonsocial stimuli on juvenile hormone (JH) titer in male burying beetles (Nicrophorus orbicollis). The initial JH response to discovery of a carcass was substantial (10-15-fold increase over controls) and rapid (<1h), and occurred whether or not a female was present. By 3h after discovery, JH titers were declining, the decline being more pronounced when a female was not present. We also tested the effect of larval stimulation on JH titer in care-giving males by removing a male's brood and replacing it with a brood of first or third instar larvae. Males initially providing care for begging first instar larvae continued to maintain high titers of JH when the replacement broods were first but not third instars. Males caring for third instar larvae (normally low JH titers) maintained low levels of JH regardless of the developmental stage of the replacement brood. This suggests that once males begin to care for nutritionally independent third instar larvae, JH titers remain low regardless of subsequent larval stimulation. Burying beetles are socially and hormonally complex organisms in which stimuli from a breeding resource, mating partners, rivals and young interact to alter the JH profile of breeding adults.     

Covert shift of attention modulates the ongoing neural activity in a reaching area of the macaque dorsomedial visual stream

Background

Attention is used to enhance neural processing of selected parts of a visual scene. It increases neural responses to stimuli near target locations and is usually coupled to eye movements. Covert attention shifts, however, decouple the attentional focus from gaze, allowing to direct the attention to a peripheral location without moving the eyes. We tested whether covert attention shifts modulate ongoing neuronal activity in cortical area V6A, an area that provides a bridge between visual signals and arm-motor control.

Methodology/Principal Findings

We performed single cell recordings from 3 Macaca Fascicularis trained to fixate straight-head, while shifting attention outward to a peripheral cue and inward again to the fixation point. We found that neurons in V6A are influenced by spatial attention. The attentional modulation occurs without gaze shifts and cannot be explained by visual stimulations. Visual, motor, and attentional responses can occur in combination in single neurons.

Conclusions/Significance

This modulation in an area primarily involved in visuo-motor transformation for reaching may form a neural basis for coupling attention to the preparation of reaching movements. Our results show that cortical processes of attention are related not only to eye-movements, as many studies have shown, but also to arm movements, a finding that has been suggested by some previous behavioral findings. Therefore, the widely-held view that spatial attention is tightly intertwined with—and perhaps directly derived from—motor preparatory processes should be extended to a broader spectrum of motor processes than just eye movements.