Factors influencing sexual performance in male rhesus monkeys.

A 5-yr retrospective study of the sexual behavior of eight adult male rhesus monkeys showed that sexual vigor declined over the years but testosterone levels in peripheral vein plasma did not. Two prospective experiments were then carried out on these males during the sixth year. (a) The four poorest performers were injected daily for 28 days with testosterone propionate (1 mg/kg of body weight). There was no significant increase in level of performance, and behavior was not correlated with plasma levels of testosterone either before or 24 hr after the last hormone injection. (b) All eight males were exposed to novel nonspecific sensory stimulation during tests of sexual behavior. Eight different adult male rhesus strangers-present in the room but not in the test cage-were used as stimuli, one for each experimental test. Sexual behavior during experimental and control tests did not differ.     

Continuity and Change in Emotional Reactivity in Rhesus Monkeys Throughout the Prepubertal Period

We examined continuity and change in emotional reactiviy as assessed by hypothalamic–pituitary–adrenal (HPA) activity in rhesus monkeys. Plasma samples were obtained from mother-peer–reared and surrogate-peer–reared monkeys and assayed for cortisol concentrations at 5 time points in infancy. Both plasma and saliva samples were collected for cortisol assay from the same monkeys as 1-, 2-, and 3-year-old juveniles, respectively. Plasma cortisol concentrations increased during the first 5 months of life and decreased from 1 to 3 years of age. Females consistently had higher plasma cortisol concentrations than males. Plasma cortisol concentrations were lower in surrogate-peer–reared than mother-peer–reared monkeys during the first month of life. Juvenile plasma cortisol concentrations were significantly correlated with infant cortisol levels at all but the earliest time point. Analysis of salivary cortisol from a subset of animals showed a similar age-related decline and the presence of a significant rearing effect, with lower concentrations in surrogate-peer–reared juveniles, but no sex difference. Salivary and plasma cortisol concentrations in these animals were significantly correlated.     

Social and nonsocial behaviors of adult rhesus monkeys after amygdalectomy in infancy or adulthood.

At 6 yr of age six female rhesus monkeys that had sustained bilateral amygdalectomy in infancy, and five intact controls, were transferred to an observation cage where behaviors were recorded while the monkeys were (a) alone, (b) paired with unfamiliar stimulus animals, and (c) paired with familiar monkeys from the opposite experimental group. The five adult controls then underwent amygdalectomy, and all tests were repeated with the infant- and adult-operated animals. Infant-operated monkeys changed behaviors more rapidly than did intact controls in social and nonsocial situations, and their activity levels were less modified after a 24-hr period in the observation cage. They were subordinate to intact controls but expressed less fear than did controls when briefly placed with an unfamiliar aggressive animal. Adult amygdalectomy produced many changes in behavior, but these aberrations were identical to those observed in like-age monkeys that had been amygdalectomized in infancy. Infant-operated monkeys demonstrated more behavioral deficits at 6 yr than they had earlier in life.     

Menstrual cycle influences on operant behavior of female rhesus monkeys.

Nine female rhesus monkeys were paired with males throughout 63 menstrual cycles. The females' motivation to approach males was studied with an operant conditioning paradigm that required the female to press a lever 250 times to gain access to the male. Sexual behavior was scored during standard 60-min tests that followed the attainment of access (17 pairs, 1,440 tests). In the overall data, mean times to access were shortest at mid-cycle and longest just before and after the onset of menstruation, and a model-fitting method showed that 45% of cycles from individual pairs were significantly correlated with a V-shaped model of the overall pattern. Male sexual activity was highest at mid-cycle and lowest in the last quarter of the cycle, but the changes in access times could not be attributed entirely to the rewarding effects of the ejaculations. In the combined data from five females (9 pairs, 33 cycles), high estradiol levels and low progesterone levels were statistically associated with short access times and short ejaculation times. The overall effect was for operant performance and sexual activity to be synchronized and maximized in the periovulatory period of the menstrual cycle.     

Return of juvenile rhesus monkeys (Macaca mulatta) to the natal social group following an 18 week separation

Return of 6 juvenile rhesus monkeys to their natal social group following an absence of 18 weeks resulted in changes in cortisol levels and absolute numbers of lymphocyte subsets 24 hours later which were related to behaviors received during the 2 hours immediately following the return. Baseline blood samples were collected 1 week prier to the return and then at 24 hours, 1 week, and 4 weeks thereafter and hermonal and immune measurements were made. Six subjects, matched for age, sex, weight, and rank, which had remained in the social group also were evaluated. In contrast to those subjects which remained in the group (“in-group”), test subjects showed significantly higher cortisol levels and significantly lower absolute numbers of T-helper and T-suppresser cells 24 hours following return when compared to baseline values. There was a significant correlation between percent decline from baseline in absolute numbers of total T cells and total frequency of bites received during the 2 hours following return to the group (r = −0.85). Additionally, mothers of the test subjects showed a significantly greater increase in cortisol levels 24 hours following return than mothers of the in-group subjects. Finally, for the test subjects, there was near perfect negative correlation between absolute numbers of total T cells and cortisol levels 24 hours following return (r = −0.95). These data demonstrate that return to a social group may be stressful and that the specific individual behavioral interactions may predict physiological responses. © 1993 Wiley-Liss, Inc.     

Inverted U-Shaped Function Between Flow and Cortisol Release During Chess Play

This study focused on the salivary cortisol level and its relation to the two components of flow (flow absorption and flow fluency) in tournament chess players exposed to one of the skill-demand-level manipulations (underload, fit, and overload). The aims of this study were to investigate how skill-demand-level manipulations affect cortisol release and how flow and cortisol release are related in the context of an engaging task. Specifically, the task involved fifty-seven tournament chess players playing chess against a software in one of the experimental groups. We assessed flow after chess playing for 25 min via questionnaire and collected saliva before chess playing (T1), right after chess playing (T2), and 10 min after T2 (T3). Our findings show that cortisol levels were affected by the skill-demand-level manipulations. At T3, participants in the overload group showed higher cortisol levels than participants in the fit and underload groups. There were no differences in cortisol release between the experimental groups at T2. In addition, we found the expected inverted U-shaped relation between cortisol release and flow absorption at T2. A moderate level of cortisol was associated with a higher level of flow absorption. In contrast, a higher level of cortisol was associated with a lower level of flow absorption. Against our expectations, flow fluency was not related to cortisol release. We discuss practical and theoretical implications of our results as well as potential for future research.     

Conditioned suppression by a stimulus associated with nalorphine in morphine-dependent monkeys

Three rhesus monkeys, physically dependent on morphine, were trained to press a lever for food on a fixed ratio of 10 responses. A tone, initially a neutral stimulus, was aperiodically presented every third or fourth session, 5 min before and after the intravenous injection of nalorphine, a morphine antagonist which produces an immediate withdrawal syndrome in morphine-dependent monkeys. After several sessions, conditioned suppression of food-lever response rate was observed. Conditioned bradycardia, emesis, and excessive salivation also occurred. In 40 to 45 sessions the conditioned suppression of food-lever response rate and the conditioned autonomic changes were extinguished by presenting pairings of a tone and saline injection. The monkeys were then reconditioned by presenting the tone aperiodically, every third or fourth session, 5 min before and after the intravenous injection of nalorphine. Results were similar to the initial conditioning sessions. Two rhesus monkeys not dependent on morphine were stabilized on a food schedule similar to that used for the first three monkeys. These monkeys showed no change in food-lever response rate during or after nalorphine injections.     

Cognitive functioning and cortisol profiles in first episode major depression

Major Depressive Disorder (MDD) is often associated with high levels of stress and disturbances in the Hypothalamic Pituitary Adrenal (HPA) system, yielding high levels of cortisol, in addition to cognitive dysfunction. Previous studies have shown a relationship between cortisol profile and cognitive functioning in recurrent MDD in general. More specifically, the association between hypercortisolism and cognitive functioning, such as memory and Executive Functioning (EF), and also more recently cortisol suppression has been explored. However, no studies have investigated these relationships in patients diagnosed with first episode MDD. The aim of the present study was to examine the relationship between cortisol levels before and after the Dexamethasone suppression test (DST) and cognitive function in first episode MDD patients. Twenty‐one patients meeting the DSM‐IV criteria for a first episode of MDD diagnosis were included in the study. The control group was matched for age, gender and education level. Cortisol was measured in saliva collected with Salivette sampling devices. Saliva samples were collected 4 times during a 24 hours period over two consecutive days: at awakening, after 45 minutes, after 7 hours and at 11 pm. Dexamethasone (1.0 mg) was given orally on Day 1 at 11 pm. The neuropsychological test battery consisted of standardized tests measuring executive functioning (EF) and memory functioning. Cortisol levels did not differ significantly between patients and controls on Day 1, except for the last sample before Dexamethasone administration, where the control group showed higher levels. Both groups showed suppression after Dexamethasone. On Day 2 there was a significant difference between groups at the third sample, showing a significantly lower level in the control group, suggesting that the controls have a more effective suppression profile than the patients. There were no significant correlations between cortisol levels before or after Dexamethasone and cognitive measures. The results indicate impairment on HPA‐axis functioning in first episode MDD patients, with less suppression functioning compared to healthy controls, but no relationship between cortisol profile and cognitive functioning in EF or Memory.     

A follow-up of cognitive performance and diurnal salivary cortisol changes in former burnout patients

The purpose of this study was to determine whether recovery from burnout is associated with improved cognitive functioning, and whether such improvement is associated with changes in hypothalamic-pituitary-adrenal axis activity and return to work. Forty-five former burnout patients were followed up after 1.5 years with a neuropsychological examination, diurnal salivary cortisol measurements, dexamethasone suppression test (DST), and self-ratings of cognitive problems. At follow-up, improved cognitive performance was observed on several tests of short-term memory and attention. Self-rated cognitive problems decreased considerably, but this decrease was unrelated to the improvement on neuropsychological tests. Diurnal salivary cortisol concentrations at awakening, 30?min after awakening, and in the evening, did not change from baseline to follow-up, nor did the cortisol awakening response. However, slightly, but significantly, stronger suppression of cortisol in response to the DST was observed at follow-up. Improvements in subjective or objective cognitive functioning and changes in diurnal cortisol concentration were unrelated to the extent of work resumption. However, a decreased DST response at follow-up was partially related to improved cognitive performance and work resumption. The clinical implications are that burnout seems to be associated with slight and significantly reversible cognitive impairment, and that self-rated cognitive change during recovery poorly reflects objective cognitive change.     

Moderate psychosocial stress appears not to impair recall of words learned 4 weeks prior to stress exposure

Recent studies in humans have reported that recall of previously learned material is especially sensitive to the disruptive effects of pharmacologically induced cortisol elevations. Whether similar effects occur after exposure to psychosocial stress remains to be shown. Moreover it is unknown whether stress before or after the initial learning interacts with the later effects of repeated stress on delayed recall (e.g. state-dependent learning). Forty subjects participated in the present experiment. They learned a word list either one hour before or 10 min after exposure to a psychosocial laboratory stressor. Delayed recall was tested 4 weeks later, again either before or after stress. Salivary cortisol levels increased significantly in response to both stress exposures. Stress had no effects on the initial learning and also did not impair delayed recall. Moreover there was no evidence for state-dependent learning. The current data seem to be in conflict with previous studies demonstrating that delayed recall is especially sensitive to elevated cortisol levels. Several reasons for these discrepancies are discussed. Among them is the small sample size, the moderate cortisol increase in response to the second stress exposure but also the long recall delay, which might lead to memory traces less susceptible to stress.     

Testing complex animal cognition: Concept learning,proactive interference,and list memory

This article describes an approach for assessing and comparing complex cognition in rhesus monkeys and pigeons by training them in a sequence of synergistic tasks, each yielding a whole function for enhanced comparisons. These species were trained in similar same/different tasks with expanding training sets (8, 16, 32, 64, 128 … 1024 pictures) followed by novel‐stimulus transfer eventually resulting in full abstract‐concept learning. Concept‐learning functions revealed better rhesus transfer throughout and full concept learning at the 128 set, versus pigeons at the 256 set. They were then tested in delayed same/different tasks for proactive interference by inserting occasional tests within trial‐unique sessions where the test stimulus matched a previous sample stimulus (1, 2, 4, 8, 16 trials prior). Proactive‐interference functions revealed time‐based interference for pigeons (1, 10 s delays), but event‐based interference for rhesus (no effect of 1, 10, 20 s delays). They were then tested in list‐memory tasks by expanding the sample to four samples in trial‐unique sessions (minimizing proactive interference). The four‐item, list‐memory functions revealed strong recency memory at short delays, gradually changing to strong primacy memory at long delays over 30 s for rhesus, and 10 s for pigeons. Other species comparisons and future directions are discussed.     

Penile responses of rats (Rattus norvegicus) in extended ex copula tests

Prolonged tests of rats' penile responses outside the context of copulation (ex copula) were undertaken to facilitate analysis of these penile components of copulatory behavior. Penile erections and flips were evoked for 1 hr following penile sheath retraction (SR), and rats were retested for 30 min after a rest interval of 5 min to 4 hr. The number of penile responses declined sharply over the course of the hour. Following a 5-min rest, there was little likelihood of additional responses. Within 2 hr some measures of penile response potential approached their original high asymptotes; other measures were still depressed after 4-hr rest. In control tests, the penile sheath was unretracted (SU) during the first 60 min, and hence few or no penile responses occurred. This condition caused no reduction in the number of erections and flips in the subsequent 30-min SR test; hence the reduction in response potential during and after SR tests was due to the responses displayed, not to the conditions of restraint. Ejaculation occurred frequently in the SU condition but rarely in SR tests, results suggesting that sheath retraction may normally inhibit ejaculation in ex copula tests, and perhaps during copulation as well.     

Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill.

Hand preferences were recorded for 35 rhesus monkeys (Macaca mulatta) as they manipulated a joystick in response to 2 computerized tasks. These preferences were then used to contrast 8 left- and 10 right-handed subjects on performance measures of hand skill. Individual hand preferences were found, but no significant population asymmetry was observed across the sample. However, the performance data reveal substantial benefits of right-handedness for joystick manipulation, as this group of monkeys mastered the 2 psychomotor tasks significantly faster than did their left-handed counterparts. The data support earlier reports of a right-hand advantage for joystick manipulation and also support the importance of distinguishing between hand preference and manual performance in research on functional asymmetries.     

Conditioned behavioral and physiological changes associated with injections of a narcotic antagonist in morphine-dependent monkeys

Environmental stimuli which are repeatedly associated with the nalorphine-induced withdrawal syndrome in morphine-dependent monkeys acquire the ability to produce a variety of conditioned behavioral and physiological responses. Morphine-dependent rhesus monkeys were studied under a fixed-ratio schedule where every tenth lever press produced a food pellet. After several pairings of a stimulus (light or tone) with intravenous injection of a dose of nalorphine which produced an immediate and severe withdrawal syndrome, onset of the stimulus alone produced conditioned suppression of lever pressing, heartrate decrease, vomiting and salivation. Conditioned suppression of responding and conditioned heart-rate changes persisted in post-dependent monkeys for one to four months after termination of chronic morphine treatment. No conditioned electrocardiogram, respiration or temperature changes were ever seen. A second group of morphine-dependent rhesus monkeys was studied under a schedule where every lever press produced an intravenous injection of morphine. After 10 pairings of a light with the intravenous injection of a dose of nalorphine which produced marked withdrawal signs and increased responding for morphine, presentation of the light and injection of sahne produced conditioned increases in responding for morphine. A third group of morphine-dependent rhesus monkeys was studied under a schedule where every nth lever press (n = 1 to 10) terminated a stimulus light associated with periodic injections of nalorphine or naloxone; lever-press responding was engendered and subsequently maintained. Thus, stimuli associated with the nalorphineor naloxone-induced withdrawal syndrome can either suppress, enhance or maintain behavior depending on the schedule conditions.     

Neuroendocrine responses to psychological stress in eumenorrheic and oligomenorrheic women

Neuroendocrine adaptive responses to psychological stress include activation of the hypothalamic-pituitary-adrenal (HPA) axis and sometimes suppression of the hypothalamic-pituitary-gonadal (HPG) axis. In women who experience chronic stress, these responses are probably responsible for disturbances in the menstrual cycle. In the present experiment, we investigated the effect of an acutely stressful situation on the physiological and neuroendocrine responses in college age women. We hypothesized that females who are experiencing some degree of abnormal menstrual function or women who have less-robust cycles (oligomenorrheic females) would exhibit differences in gonadotropin secretion from eumenorrheic females when exposed to psychological stressors. Fifteen women completed this study: eumenorrheic (n = 5) and oligomenorrheic women (n = 5) who experienced a series of psychological stressors, and eumenorrheic controls (n = 5). Blood samples were taken at 10 min intervals for 8 h (09:00-17:00) in each woman during the mid-follicular phase of the menstrual cycle. The psychological stressors were administered for 1 h beginning at 13:00 h. Luteinizing hormone (LH), growth hormone (GH) and cortisol were measured in each sample to assess the effect of stress on secretion of these hormones. Deconvolution analysis was used to analyze pulsatile hormone secretion and the approximate entropy (ApEn) statistic analyzed the regularity of release of each hormone. Although, there were significant changes in heart rate (HR), skin resistance (SR) and cortisol levels in the stressed women during the psychological stressor compared to resting baseline values but not in the controls, there was no difference in either LH or GH secretion between women who experienced stress and those who did not. Furthermore, there were no differences in the LH or GH secretion patterns in the oligomenorrheic and eumenorrheic women exposed to the psychological stressor.     

Sequential responding and planning in capuchin monkeys (Cebus apella)

Previous experiments have assessed planning during sequential responding to computer generated stimuli by Old World nonhuman primates including chimpanzees and rhesus macaques. However, no such assessment has been made with a New World primate species. Capuchin monkeys (Cebus apella) are an interesting test case for assessing the distribution of cognitive processes in the Order Primates because they sometimes show proficiency in tasks also mastered by apes and Old World monkeys, but in other cases fail to match the proficiency of those other species. In two experiments, eight capuchin monkeys selected five arbitrary stimuli in distinct locations on a computer monitor in a learned sequence. In Experiment 1, shift trials occurred in which the second and third stimuli were transposed when the first stimulus was selected by the animal. In Experiment 2, mask trials occurred in which all remaining stimuli were masked after the monkey selected the first stimulus. Monkeys made more mistakes on trials in which the locations of the second and third stimuli were interchanged than on trials in which locations were not interchanged, suggesting they had already planned to select a location that no longer contained the correct stimulus. When mask trials occurred, monkeys performed at levels significantly better than chance, but their performance exceeded chance levels only for the first and the second selections on a trial. These data indicate that capuchin monkeys performed very similarly to chimpanzees and rhesus monkeys and appeared to plan their selection sequences during the computerized task, but only to a limited degree.     

An assessment of memory awareness in tufted capuchin monkeys (Cebus apella)

Humans, apes, and rhesus monkeys demonstrate memory awareness by collecting information when ignorant and acting immediately when informed. In this study, five capuchin monkeys searched for food after either watching the experimenter bait one of four opaque tubes (seen trials), or not watching (unseen trials). Monkeys with memory awareness should look into the tubes before making a selection only on unseen trials because on seen trials they already know the location of the food. In Experiment 1, one of the five capuchins looked significantly more often on unseen trials. In Experiment 2, we ensured that the monkeys attended to the baiting by interleaving training and test sessions. Three of the five monkeys looked more often on unseen trials. Because monkeys looked more often than not on both trial types, potentially creating a ceiling effect, we increased the effort required to look in Experiment 3, and predicted a larger difference in the probability of looking between seen and unseen trials. None of the five monkeys looked more often on unseen trials. These findings provide equivocal evidence for memory awareness in capuchin monkeys using tests that have yielded clear evidence in humans, apes, and rhesus monkeys.     

Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where,but not when,in an open-field test of memory

We adapted a paradigm developed by Clayton and Dickinson (1998), who demonstrated memory for what, where, and when in scrub jays, for use with rhesus monkeys. In the study phase of each trial, monkeys found a preferred and a less-preferred food reward in a trial-unique array of three locations in a large room. After 1 h, monkeys returned to the test room, where they found foods placed as during study. Twenty-five hours after the study phase monkeys again searched the room, but now the preferred food was replaced with a distasteful food remnant, while the less-preferred food was still present. Although monkeys remembered the locations of the foods for up to 25 h, they did not learn that the preferred food was available after the short, but not after the long delay. Thus, monkeys demonstrated long-term memory for the type and location of food but failed to demonstrate sensitivity to when they acquired that knowledge.     

Interaction between penile reflexes and copulation in male rats

Intact, unanesthetized male rats were place in a supine position, with the penile sheath continuously retracted. Three forms of penile reflex were displayed: erections, cups, and flips. The reciprocal relation between copulation and the penile reflexes occurring in supine tests was explored in four experiments. In Experiment 1, sexual exhaustion depressed all penile reflexes, but the reflexes returned to baseline levels within 8 hr, long before copulatory potential. In Experiment 2, reflexes were depressed to exhaustion levels after fewer ejaculations than were required for sexual exhaustion, an indication that reflexes are more readily evoked during copulation than in supine tests. Experiment 3 determined that a rat's penile-reflex potential may be enhanced by placing the rat in a copulation-test cage, by allowing the male a few antecedent intromissions, or by allowing an antecedent ejaculation. The display of penile reflexes within 1 min after ejaculation suggests that the period of reduced sexual arousability following ejaculation is not due to reduced excitability in the spinal mechanisms controlling penile reflexes. In Experiment 4, 1 hr of penile-reflex elicitation had no effect on subsequent copulatory behavior. Thus, sexual stimulation may increase or decrease penile-reflex potential, but a reciprocal influence was not detectable.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) show robust evidence for memory awareness across multiple generalization tests

The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton in Proc Natl Acad Sci USA 98:5359–5362, 2001; Smith et al. in Behav Brain Sci 26:317–374, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.