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Pierre Lavenex

Publications and source records attributed to Pierre Lavenex.

9 recordsLinked to original sources

Postnatal development of the primate hippocampal formation.

The hippocampal formation is a multicomponent region of the medial temporal lobe preferentially involved in declarative and relational memory processing. Behavioral studies have suggested a protracted functional maturation of these structures in primates, and postnatal developmental abnormalities in the hippocampal formation are thought to contribute to neurodevelopmental disorders, such as autism, schizophrenia, epilepsy and Down syndrome. Despite all that we know about the functional organization of the adult hippocampal formation, notably absent is a systematic study of its postnatal maturation in primates. In this article, we review current knowledge of the structural development of the primate hippocampal formation and present new data on its postnatal neuroanatomical development. We summarize what is known about the neurobiological processes, such as the addition of new neurons, the establishment and elaboration of connectivity, and the neurochemical changes, that underlie the structural development and functional maturation of the primate hippocampal formation. We conclude that there is yet insufficient information to identify distinct developmental windows during which different hippocampal regions undergo specific maturational processes. For this reason, it is currently impossible to determine the ages at which specific hippocampal circuits become structurally mature and potentially capable of supporting defined, age-specific functional processes. Together with work in rodents, systematic studies of the structural development and functional maturation of the monkey hippocampal formation will be necessary to gain insight not only into the types of information processing that it subserves, but also into the specific maturational processes that might be affected in human neurodevelopmental disorders.

Aging↗

Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys.

The hippocampus is important for the acquisition of spatial representations of the environment and consequently in contextual memory. This suggests that the neural substrates underlying spatial cognition might be essential for remembering specific life episodes. Indeed, hippocampal lesions prevent spatial relational learning in adult rodents and monkeys, and result in profound amnesia in adult humans. In contrast, we show here that monkeys with neonatal hippocampal lesions learned new spatial relational information. Our experiments suggest that early hippocampal damage leads to functional brain reorganization that enables spatial information to be acquired through the use of brain regions that normally do not subserve this function.

Adaptation, Physiological↗

Hippocampal lesion prevents spatial relational learning in adult macaque monkeys.

The role of the hippocampus in spatial learning and memory has been extensively studied in rodents. Comparable studies in nonhuman primates, however, are few, and findings are often contradictory. This may be attributable to the failure to distinguish between allocentric and egocentric spatial representations in experimental designs. For this experiment, six adult monkeys received bilateral hippocampal ibotenic acid lesions, and six control subjects underwent sham surgery. Freely moving monkeys then foraged for food located in two arrays of three distinct locations among 18 locations distributed in an open-field arena. Multiple goals and four pseudorandomly chosen entrance points precluded the monkeys' ability to rely on an egocentric strategy to identify food locations. Monkeys were tested in two conditions. First, local visual cues marked the food locations. Second, no local cues marked the food locations, so that monkeys had to rely on an allocentric (spatial relational) representation of the environment to discriminate these locations. Both hippocampal-lesioned and control monkeys discriminated the food locations in the presence of local cues. However, in the absence of local cues, control subjects discriminated the food locations, whereas hippocampal-lesioned monkeys were unable to do so. Interestingly, histological analysis of the brain of one control monkey whose behavior was identical to that of the experimentally lesioned animals revealed a bilateral ischemic lesion restricted to the hippocampus. These findings demonstrate that the adult monkey hippocampal formation is critical for the establishment or use of allocentric spatial representations and that selective damage of the hippocampus prevents spatial relational learning in adult nonhuman primates.

Animals↗

Spatial relational memory in 9-month-old macaque monkeys.

This experiment assesses spatial and nonspatial relational memory in freely moving 9-mo-old and adult (11-13-yr-old) macaque monkeys (Macaca mulatta). We tested the use of proximal landmarks, two different objects placed at the center of an open-field arena, as conditional cues allowing monkeys to predict the location of food rewards hidden in one of two sets of three distinct locations. Monkeys were tested in two different conditions: (1) when local visual cues marked the two sets of potentially baited locations, so that monkeys could use both local and spatial information to discriminate these locations from never-baited locations; and (2) when no local visual cues marked the two sets of potentially baited locations, so that monkeys had to rely on a spatial relational representation of the environment to discriminate these locations. No 9-mo-old or adult monkey associated the presence of the proximal landmarks, at the center of the arena, with the presence of food in one set of three distinct locations. All monkeys, however, discriminated the potentially baited locations in the presence of local visual cues, thus providing evidence of visual discrimination learning. More importantly, all 9-mo-old monkeys tested discriminated the potentially baited locations in absence of the local visual cues, thus exhibiting evidence of spatial relational learning. These findings indicate that spatial memory processes characterized by a relational representation of the environment are present as early as 9 mo of age in macaque monkeys.

Age Factors↗

Nutritional deficits during early development affect hippocampal structure and spatial memory later in life.

Development rates vary among individuals, often as a result of direct competition for food. Survival of young might depend on their learning abilities, but it remains unclear whether learning abilities are affected by nutrition during development. The authors demonstrated that compared with controls, 1-year-old Western scrub jays (Aphelocoma californica) that experienced nutritional deficits during early posthatching development had smaller hippocampi with fewer neurons and performed worse in a cache recovery task and in a spatial version of an associative learning task. In contrast, performance of nutritionally deprived birds was similar to that of controls in 2 color versions of an associative learning task. These findings suggest that nutritional deficits during early development have long-term consequences for hippocampal structure and spatial memory, which, in turn, are likely to have a strong impact on animals' future fitness.

Age Factors↗

Perirhinal and parahippocampal cortices of the macaque monkey: Intrinsic projections and interconnections.

We investigated the topographic and laminar organization of the intrinsic projections and interconnections of the macaque monkey perirhinal and parahippocampal cortices. Discrete anterograde tracer injections placed at various rostrocaudal and mediolateral levels in these cortices revealed extensive associational connections both within and between the perirhinal and parahippocampal cortices. Areas 35, 36rm, 36rl, 36cm, and 36cl are highly interconnected, whereas area 36d (encompassing the dorsal portion of the medial temporal pole) shares only modest connections with the rest of the perirhinal cortex. Areas TH, TFm, and TFl of the parahippocampal cortex also share an extensive network of associational connections that tend to be heaviest within a given subdivision. Area 36c of the perirhinal cortex is the main interface between the perirhinal and parahippocampal cortices. Its heaviest connections are with area 36r and the anterior aspect of area TF. The laminar organization of all these connections is typical of associational projections. Anterograde tracer experiments revealed that these projections are distributed through both deep and superficial layers, although heavier projections are directed toward the superficial layers. Results of retrograde tracer experiments suggested that the projections from caudal areas (36c or TF) to area 36r are of the feedforward type, whereas the projections from areas 36r and 36c to area TF are of the feedback type. These findings suggest that the perirhinal cortex is at a higher level than the parahippocampal cortex in the hierarchy of associational cortices. We discuss the functional implications of the organization of these extensive networks of intrinsic, associational projections.

Animals↗

Nonphosphorylated high-molecular-weight neurofilament expression suggests early maturation of the monkey subiculum.

We analyzed the distribution of nonphosphorylated high-molecular-weight neurofilaments (NF-H) in the hippocampal formation of infant (3-week-old and 3-month-old) and adult (9-17-year-old) macaque monkeys in order to obtain neuroanatomical evidence of the maturity of these structures shortly after birth. We employed the monoclonal antibody SMI-32, a well-characterized antibody raised against nonphosphorylated NF-H, the expression of which is believed to reflect the maturation of certain neuronal populations. Patterns of SMI-32 immunoreactivity differed dramatically between infant and adult monkeys. In adults, nonphosphorylated NF-H expression was prominent in the CA3 and CA2 fields of the hippocampus, in the subiculum and in the entorhinal cortex. In infants, only the subiculum stained heavily for nonphosphorylated NF-H. These findings suggest that different subregions of the primate hippocampal formation mature at different times during development. The subiculum, the major source of efferent projections from the hippocampal formation toward subcortical structures, matures early during development. In contrast, the entorhinal cortex, the main interface of the hippocampal formation with the neocortex, matures relatively later. These findings have direct implications for the type of information processing that might be subserved by the primate hippocampal formation shortly after birth, as well as for the emergence of particular behavioral and memory processes during postnatal development.

Aging↗

The amygdala: is it an essential component of the neural network for social cognition?

Observations from human subjects with focal brain lesions and animal subjects with experimental lesions have implicated a variety of brain regions in the mediation of social behavior. Previous studies carried out in the macaque monkey found that lesions of the amygdala not only decrease emotional reactivity but also disrupt normal social interactions. We have re-investigated the relationship between amygdala lesions and social behavior in cohorts of mature and neonatal rhesus monkeys who were prepared with selective and complete bilateral ibotenic acid lesions of the amygdaloid complex. These animals display clear alterations in emotional and social behavior. We interpret these changes as due to a loss of the ability to evaluate environmental stimuli as potential threats. However, adult animals with bilateral lesions of the amygdala demonstrate near normal, and even increased, social interactions with conspecifics. Moreover, neonatal animals, prepared with amygdala lesions at 2 weeks of age, also demonstrate species typical social behaviors such as the generation of facial expressions, grooming and play behavior. These results argue against the idea that the amygdala is essential for the interpretation of social communication or for the expression of social behavior. Because it does appear to participate in the evaluation of the "safety" of social interactions, we believe that it does have a role in modulating the amount of social behavior in which an organism will participate. However, our current answer to the question posed in the title of this paper is no!

Amygdala↗

Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex.

We investigated the topographic and laminar organization of the efferent cortical projections of the perirhinal and parahippocampal cortices. Area 36 of the perirhinal cortex projects preferentially to areas TE and TEO, whereas area TF of the parahippocampal cortex projects preferentially to the posterior parietal cortex and area V4. Area TF projects to many regions of the frontal lobe, whereas area 36 projects mainly to the orbital surface. The insular and cingulate cortices receive projections from areas 36 and TF, whereas only area TF projects to the retrosplenial cortex. Projections to the superior temporal gyrus, including the dorsal bank of the superior temporal sulcus, arise predominantly from area TF. Area 36 projects only to rostral levels of the superior temporal gyrus. Area TF has, in general, reciprocal connections with the neocortex, whereas area 36 has more asymmetric connections. Area 36, for example, projects to more restricted regions of the frontal cortex and superior temporal sulcus than it receives inputs from. In contrast, it projects to larger portions of areas TE and TEO than it receives inputs from. The efferent projections of areas 36 and TF are primarily directed to the superficial layers of the neocortex, a laminar organization consistent with connections of the feedback type. Projections to unimodal visual areas terminate in large expanses of the cortex, but predominantly in layer I. Projections to other sensory and polymodal areas, in contrast, terminate in a columnar manner predominantly in layers II and III. In all areas receiving heavy projections, the projections extend throughout most cortical layers, largely avoiding layer IV. We discuss these findings in relation to current theories of memory consolidation.

Amino Acids↗