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Jocelyne Bachevalier

Publications and source records attributed to Jocelyne Bachevalier.

17 recordsLinked to original sources

Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex.

Non-human primates, like humans, develop and maintain social relationships and attachments throughout their life. The first and most crucial relationship in a primate life is that with its mother. Yet, in absence of their biological mother, infant primates form attachment to surrogate mothers. Although, this early attachment is critical for the development of normal species-typical social and emotional skills, the neural substrates underlying the formation of social relationships in primates are still unclear. The present study assessed, in infant rhesus monkeys (Macaca mulatta) reared by human caregivers and social interactions with peers, the effects of bilateral neonatal (1-2 weeks of age) ibotenic acid lesions of the amygdala and hippocampus (N=6 in each group), aspiration lesions of the orbital frontal cortex (N=6) or sham lesions (N=5) on the development of a social attachment with the principal human caregiver. A specific preference for the later was assessed at 11 months of age, in a two-choice discrimination task, opposing the principal human caregiver to another familiar human, in a familiar environment. None of the lesions impaired the expression of preferential responses toward the principal human caregiver. Nevertheless, lesions of the orbital frontal cortex led to a weaker preference, suggesting that this structure may play a role in the quality and/or strength of the infant/mother relationships. The present non-human primate findings are discussed in terms of their relevance for autism.

Amygdala↗

Responses to affective stimuli in monkeys with entorhinal or perirhinal cortex lesions.

Recent efforts to define the functions of the primate rhinal (entorhinal and perirhinal) cortical areas have focused on their interaction with the hippocampus in the mediation of normal memory. Less is known on the functional meaning of their strong connections to the amygdala, a key substrate for emotion. A previous study (Meunier and Bachevalier, 2002) showed evidence that complete rhinal ablations yield changes in monkeys' behavioral responses to affectively salient stimuli. Here, we studied monkeys with separate entorhinal or perirhinal ablations in the same paradigm, where responses were triggered by four stimuli: an unfamiliar human, a conspecific stimulus, a toy snake, and a familiar (generally rewarded) junk object. The two separate lesions produced similar changes, and each replicated the effects of complete rhinal lesions (i.e., attenuated affiliation and enhanced defense). Failure to modulate responses based on previous experience (i.e., memory difficulties) may explain these affective changes. This interpretation does not account, however, for the sparing of some memory-dependent modulations of defense, nor for the lack of correlation between the animals' affective changes and their own recognition memory performance. Alternatively, rhinal damage may introduce a negative bias in the risk assessment of affectively salient stimuli, a proposal more compatible with Gray and McNaughton's (2000) anxiety-centered view of medial temporal functions, than with prominent mnemonic/perceptual functional models of the hippocampal/rhinal duo. Reconciling the two perspectives may improve our understanding of rhinal functions.

Affect↗

The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta).

Social dominance, personality ratings, and frequency, duration, and timing of social behaviors were measured pre- and postsurgically in 6 groups of rhesus monkeys (Macaca mulatta), each consisting of 1 sham-operated control and 1 monkey each with a selective amygdala, hippocampal, or orbital frontal cortex lesion. Unlike previous reports, none of the operated groups showed changes in social dominance postsurgery, although changes in other measures varied by lesion site. Although sham-operated monkeys displayed heightened avoidant, anxious, and aggressive behaviors, those with hippocampal lesions also showed increased exploration and excitability, along with reduced responses to affiliative signals. Amygdala lesions yielded several personality changes that precluded positive social interactions (increased exploration and excitability, decreased affiliation and popularity) and altered responses to threatening social signals. By contrast, monkeys with orbital frontal lesions were involved in more aggressive interactions and responded differently to both affiliative and threatening signals. Although several findings differ from earlier nonhuman primate studies, they are largely in agreement with human data and emphasize the context-specific nature of social behavior studies. Interpretation of results in relation to cognitive processes mediated by each structure is discussed.

Aggression↗

The amygdala and development of social cognition: theoretical comment on Bauman, Toscano, Mason, Lavenex, and Amaral (2006).

Nonhuman primate studies, using selective amygdala lesions that spare cortical areas and fibers of passage, have helped to clarify the amygdala's specific contribution to social and emotional behavior. M. D. Bauman, J. E. Toscano, W. A. Mason, P. Lavenex, and D. G. Amaral (2006) reported that macaque monkeys (Macaca mulatta) with neonatal neurotoxic amygdala lesions displayed lower rank in social dominance status, reduced aggressive gestures, and enhanced fearful reactions to social cues compared with normal controls and those with neonatal hippocampal lesions when tested as juveniles in a group of peers. These results are discussed in light of a recent study (C. J. Machado & J. Bachevalier, 2006) showing that the same selective amygdala damage in adolescent monkeys did not alter presurgical social dominance status. This variability in behavioral changes after selective amygdala lesions underscores the significant interplay between timing of the lesion, genetic traits, and environmental factors and suggests that the amygdala is not the generator of specific emotional responses, but acts as a modulator to ensure that emotional responses are appropriate to the external stimuli and social context.

Amygdala↗

The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism.

Individuals with an autistic spectrum disorder are impaired not only in understanding others' mental states, but also in self-regulation of social-emotional behavior. Therefore, a model of the brain in autism must encompass not only those brain systems that subserve social-cognitive and emotional functioning, but also those that subserve the self-regulation of behavior in response to a changing social environment. We present evidence to support the hypothesis that developmental dysfunction of the orbitofrontal-amygdala circuit of the brain is a critical factor in the development of autism and that some of the characteristic deficits of persons with autism in socio-emotional cognition and behavioral self-regulation are related to early dysfunction of different components of this circuit. A secondary hypothesis posits that the degree of intellectual impairment present in individuals with autism is directly related to the integrity of the dorsolateral prefrontal-hippocampal circuit of the brain. Together, these hypotheses have the potential to help explain the neurodevelopmental basis of some of the primary manifestations of autism as well as the heterogeneity of outcomes.

Amygdala↗

Comparison of the effects of damage to the perirhinal and parahippocampal cortex on transverse patterning and location memory in rhesus macaques.

Monkeys with damage to the parahippocampal (TH/TF) or perirhinal (PRh) cortex were tested on two sets of the transverse patterning (TP) problem (A+/B-, B+/C-, C+/A- and D+/E-, E+/F-, F+/D-) and delayed nonmatching-to-location paradigm (DNML), with delays ranging from 10 to 600 s. Damage to either area impaired acquisition and performance of TP but not of linear discriminations (e.g., A>B>C>X). Damage to areas TH/TF impaired performance of the DNML at all delays but only affected memory for objects at the longest delay, as measured by a delayed nonmatching-to-sample task (DNMS) (Nemanic et al., 2004). Damage to the PRh impaired performance of the DNMS but not of the DNML. The results present a dissociation in object and place memory for these two cortical regions and suggest a role for each in the cortical circuitry supporting configural/relational memory.

Animals↗

Selective neurotoxic damage to the hippocampal formation impairs performance of the transverse patterning and location memory tasks in rhesus macaques.

Monkeys with neurotoxic (ibotenic acid) damage to the hippocampal formation and unoperated controls were trained on two sets of transverse patterning problems (A+/B-, B+/C-, C+/A-, and D+/E-, E+/F-, F+/D-) and a delayed nonmatching-to-location paradigm (DNML) with delays of 10s, 30s, 120s, and 600s. Hippocampal lesions produced a size- and area-dependent impairment on transverse patterning. Damage largely limited to the right hippocampus in one subject had no effect on performance on the task. Of the remaining four subjects, two with hippocampal damage greater than 40% bilaterally were unable to solve the two transverse patterning sets, but could solve the linear set of discriminations (A+/B-, B+/C-, C+/X-). The two remaining operated animals were impaired in acquisition of both sets, but were eventually able to solve one of the two transverse patterning discrimination sets. All five operated monkeys were impaired relative to normal controls on DNML, but not on the standard delayed nonmatching-to-sample (DNMS) version with trial-unique objects. The results confirm our previous findings (Alvarado et al., Hippocampus 12:421-433, 2002) using aspiration lesions of the hippocampal formation and strengthen the view that the hippocampal formation is critical for object and spatial relational memory.

Animals↗

The primate hippocampus: ontogeny, early insult and memory.

Recent evidence suggests that in primates, as in rodents, the hippocampus shows a developmental continuum that affects memory abilities from infancy to adulthood. In primates relatively few hippocampal-dependent abilities (e.g. some aspects of recognition memory) are present in early infancy, whereas others (e.g. relational memory) begin to show adult-like characteristics around 2 years of age in monkeys and 5-7 years in humans. Profound and persistent memory loss resulting from insult to the hippocampus in infancy becomes evident in everyday behavior only later in childhood. This pattern of results suggests a maturational gradient within the medial temporal lobe memory system, with most abilities crucially dependent upon the hippocampus emerging in later stages of development, supporting a model of hierarchical organization of memory within the medial temporal lobe.

Animals↗

Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury.

In vivo MRI volumetric analysis enables investigators to evaluate the extent of tissue loss following traumatic brain injury (TBI). However, volumetric studies of pediatric TBI are sparse, and there have been no volumetric studies to date in children examining specific subregions of the prefrontal and temporal lobes. In this study, MRI volumetry was used to evaluate brain volume differences in the whole brain, and prefrontal, temporal, and posterior regions of children following moderate to severe TBI as compared to uninjured children of similar age and demographic characteristics. The TBI group had significantly reduced whole brain, and prefrontal and temporal regional tissue volumes as well as increased cerebrospinal fluid (CSF). Confidence interval testing further revealed group differences on gray matter (GM) and white matter (WM) in the superior medial and ventromedial prefrontal regions, WM in the lateral frontal region, and GM, WM, and CSF in the temporal region. Whole brain volume and total brain GM were reduced, and total ventricular volume, total CSF volume, and ventricle-to-brain ratio (VBR) were increased in the TBI group. Additional analyses comparing volumetric data from typically developing children and subgroups of TBI patients with and without regional focal lesions suggested that GM loss in the frontal areas was primarily attributable to focal injury, while WM loss in the frontal and temporal lobes was related to both diffuse and focal injury. Finally, volumetric measures of preserved frontotemporal tissue were related to functional recovery as measured by the Glasgow Outcome Scale (adapted for children) with greater tissue preservation predicting better recovery.

Adolescent↗

The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys.

Recognition memory was assessed by submitting the same adult monkeys to visual paired comparison (VPC) with mixed delays (10-120 sec), followed by three consecutive versions of object-delayed nonmatching-to-sample (DNMS): increasing delays (10-600 sec), lengthened lists (3-10 objects), and intervening distractors in the delays (light at 10 sec, motor task at 30-600 sec, or context change at 600 sec). Four groups were tested: normal controls, monkeys with ibotenic acid lesions of the hippocampal formation (H), and monkeys with aspiration lesions of either the perirhinal (PRh) or parahippocampal (areas TH/TF) cortex. Group H was impaired on VPC at delays > or =60 sec but had difficulty on DNMS only at 600 sec delays with distraction. In group TH/TF, the VPC impairment emerged earlier (30 sec); yet, once the nonmatching rule was mastered, no significant change occurred on any DNMS condition. Only group PRh behaved congruently on VPC and DNMS, exhibiting a deficit at the easiest condition that worsened with increasing delays as well as in DNMS lengthened list and distraction conditions. These results led us to postulate that VPC and DNMS, as previously administered to monkeys, were not equivalent visual recognition memory probes. Specifically, we propose that, for VPC, because of passive (incidental) encoding, the animal's performance rests on both item familiarity and event recollection, whereas, for DNMS, because of active (purposeful) encoding, performance relies more on item familiarity. This proposal converges with current models postulating distinct, but interactive, mnemonic roles for the hippocampal and adjacent TH/TF regions.

Animals↗

Reactions to familiar and novel objects in infant monkeys with neonatal temporal lesions.

Adult monkeys with late temporal lobe damage are known to touch and mouth objects compulsively, even unknown objects. To determine whether infants with early temporal damage display this symptom as well, 9-month-old rhesus monkeys with neonatal ablations of either the medial temporal lobe or inferior temporal cortex were exposed to four objects, two familiar and two novel. All operated infants were less active/more withdrawn than controls and showed neither exaggerated object manipulation nor hyperorality. Furthermore, like controls, they touched novel objects less than they touched familiar ones. Thus, infants with neonatal medial or inferior temporal ablations did not display the compulsive exploration evidenced after similar lesions in adulthood and retained some ability to detect novelty despite their known memory impairments.

Animals↗

Abstract-concept learning and list-memory processing by capuchin and rhesus monkeys.

Three capuchin monkeys (Cebus apella) touched the lower of 2 pictures (same) or a white rectangle (different), increased same/different abstract-concept learning (52% to 87%) with set-size increases (8 to 128 pictures), and were better than 3 rhesus monkeys (Macaca mulatta). Three other rhesus that touched the top picture before choices learned similar to capuchins but were better at list-memory learning. Both species' serial position functions were similar in shape and changes with retention delays. Other species showed qualitatively similar shape changes but quantitatively different time-course changes. In abstract-concept learning, qualitative similarity was shown by complete concept learning, whereas a quantitative difference would have been a set-size slope difference. Qualitative similarity is discussed in relation to general-process versus modular cognitive accounts.

Animals↗

Non-human primate models of childhood psychopathology: the promise and the limitations.

Although non-human primate models have been used previously to investigate the neurobiology of several sensory and cognitive developmental pathologies, they have been employed only sparingly to study the etiology of childhood psychopathologies for which deficits in social behavior and emotion regulation are major symptoms. Previous investigations of both adult human and non-human primates have indicated that primate social behavior and emotion are regulated by a complex neural network, in which the amygdala and orbital frontal cortex play major roles. Therefore, this review will provide information generated from the study of macaque monkeys regarding the timing of normal social and emotional behavior development, the normal pattern of anatomical and functional maturation of the amygdala and orbital frontal cortex, as well as information regarding the neural and behavioral effects of early perturbations of these two neural structures. We will also highlight 'critical periods' of macaque development, during which major refinements in the behavioral repertoire appear to coincide with significant neural maturation of the amygdala and/or orbital frontal cortex. The identification of these 'critical periods' may allow one to better predict the specific behavioral impairments likely to appear after neonatal damage to one or both of these neural areas at different time points during development. This experimental approach may provide a new and important way to inform and stimulate research on childhood psychopathologies, such as autism, schizophrenia and Williams syndrome, in which the development of normal social skills and emotional regulation is severely perturbed. Finally, the promise and limitations inherent to the use of non-human primate models of childhood psychopathology will be discussed.

Amygdala↗

Assessment of locus and extent of neurotoxic lesions in monkeys using neuroimaging techniques: a replication.

In a recent study, [Hippocampus 11 (2001) 361] demonstrated that in vivo neuroimaging techniques could be used to accurately quantify the extent of neuronal damage after ibotenic acid injections in non-human primates. The present study was undertaken to replicate these findings and to further estimate whether the concentration of ibotenic acid used (10-15 mg/ml) to produce the neuronal loss did not affect the fibers coursing within or around the targeted brain area. Magnetic resonance (MR) images (T1-weighted and FLAIR) were acquired in three monkeys before and after they received neurotoxic lesions of the hippocampal formation. The postsurgical FLAIR images were taken 7-10 days after surgery to visualize the hyperintense signals produced by increased edema at the injection sites. One year post-surgically, T1-weighted images were acquired and compared with T1-weighted images obtained pre-surgery to estimate reduction in hippocampal volume resulting from neuronal loss. Estimated neuronal loss was then compared with actual cell loss found during histological evaluation of brain tissue. Both neuroimaging techniques accurately estimated the extent of hippocampal damage and damage to surrounding structures. In addition, the concentration of ibotenic acid (10 mg/ml) used in the present study did not appear to have significantly damaged or de-myelinated fibers coursing through or around the hippocampal formation. Together with the previous results of [Hippocampus 11 (2001) 361], the present data strongly demonstrate that in vivo neuroimaging techniques provide powerful tools to estimate reliably and rapidly the extent and localization of brain lesions in non-human primates.

Animals↗

Object and spatial relational memory in adult rhesus monkeys is impaired by neonatal lesions of the hippocampal formation but not the amygdaloid complex.

Adult rhesus monkeys with neonatal aspiration lesions of the hippocampal formation or the amygdaloid complex (including their respective subjacent cortices) and their age-matched controls were tested on the transverse patterning problem (A+ vs. B-, B+ vs. C- and C+ vs. A-) and a spatial version of the delayed nonmatching-to-sample (DNMS) task with delays of 10 s to 30 s, 60 s, 120 s, and 600 s. Monkeys with neonatal damage to the amygdaloid complex learned both tasks and did not differ from controls at any delay of the spatial DNMS task. Monkeys with neonatal hippocampal damage, however, were unable to learn transverse patterning, though they easily transferred to a linear series (A+ vs. B-, B+ vs. C-, and C+ vs. X-). Three of the four were also unable to reach criterion on the spatial DNMS task within the limits of testing, and the performance of all four monkeys deteriorated with increasing choice delays. The data suggest a role of the primate hippocampal region in both object and spatial relational learning.

Aging↗

Comparison of emotional responses in monkeys with rhinal cortex or amygdala lesions.

Four emotionally arousing stimuli were used to probe the behavior of monkeys with bilateral ablations of the entorhinal and perirhinal cortex. The monkeys' behavioral changes were then contrasted with those observed earlier (M. Meunier, J. Bachevalier, E. A. Murray, L. Málková, & M. Mishkin, 1999) in monkeys with either neurotoxic or aspiration lesions of the neighboring amygdala. Rhinal cortex ablations yielded several subtle behavioral changes but none of them resembled any of the disorders typically seen after amygdalectomies. The changes produced by rhinal damage took mainly the form of heightened defensiveness and attenuated submission and approach responses; that is, just the opposite of some of the most distinctive symptoms following amygdala damage. These findings raise the possibility that the rhinal cortex and amygdala have distinct, interactive functions in normal behavioral adaptation to affective stimuli.

Aggression↗

Mechanisms of same/different abstract-concept learning by rhesus monkeys (Macaca mulatta).

Experiments with 9 rhesus monkeys (Macaca mulatta) showed, for the first time, that abstract-concept learning varied with the training stimulus set size. In a same/different task, monkeys required to touch a top picture before choosing a bottom picture (same) or white rectangle (different) learned rapidly. Monkeys not required to touch the top picture or presented with the top picture for a fixed time learned slowly or not at all. No abstract-concept learning occurred after 8-item training but progressively improved with larger set sizes and was complete following 128-item training. A control monkey with a constant 8-item set ruled out repeated training and testing. Contrary to the unique-species account, it is argued that different species have quantitative, not qualitative, differences in abstract-concept learning.

Analysis of Variance↗