The hippocampus, spatial memory and food hoarding: a puzzle revisited

Behavioural ecology assumes that cognitive traits and their underlying neural substrates are shaped by natural selection in much the same way as morphological traits are, resulting in adaptation to the natural environment of the species concerned. Recently, however, the 'neuroecology' approach of attempting to gain insight into brain structure and function by testing predictions about variation in brain structure based on knowledge of the lifestyle of the animal has been criticized on the grounds that such an adaptationist view cannot provide insight into the underlying mechanisms. Furthermore, the criticism has focussed on attempts to use variation in demand for spatial memory and in hippocampal size as a basis for predicting variation in cognitive abilities. Here, we revisit this critique against the field of so-called 'neuroecology' and argue that using knowledge of the natural history of animals has lead to a better understanding of the interspecific variation in spatial abilities and hippocampal size, and to the generation of novel hypotheses and predictions.     

The hippocampus and memory: insights from spatial processing

The hippocampus appears to be crucial for long-term episodic memory, yet its precise role remains elusive. Electrophysiological studies in rodents offer a useful starting point for developing models of hippocampal processing in the spatial domain. Here we review one such model that points to an essential role for the hippocampus in the construction of mental images. We explain how this neural-level mechanistic account addresses some of the current controversies in the field, such as the role of the hippocampus in imagery and short-term memory, and discuss its broader implications for the neural bases of episodic memory.     

Human memory: The hippocampus is the key

A recent study of brain-damaged patients with various degrees of amnesia provides compelling new evidence that the hippocampus plays a vital role in the laying down of new memories. Why existing memories are also affected by hippocampal damage is particularly puzzling.     

The hippocampus and memory: a comparative and ethological perspective

During the past year, considerable progress has been made in our understanding of the wide-ranging functions of the hippocampus. Highlights include the development of new tasks with which to assess spatial/topographic memory in humans and monkeys, novel tests of relational memory in rats, and episodic-like memory tasks in birds. In addition, novel theories of hippocampal function have been developed that are notable for their applicability to both humans and animal models.     

The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison

It has been hypothesized that memory-demanding ecological conditions might result in enhanced memory and an enlarged hippocampus, an area of the brain involved in memory processing, either via extensive memory experience or through evolutionary changes. Avian migration appears to represent one of such memory-demanding ecological conditions. We compared two subspecies of the white-crowned sparrow: migratory Zonotrichia leucophrys gambelii and non-migratory Z. l. nuttalli. Compared to non-migratory Z. l. nuttalli, migratory Z. l. gambelii showed better memory performance on spatial one-trial associative learning tasks and had more hippocampal neurons. Migratory subspecies also had larger hippocampi relative to the remainder of the telencephalon but not relative to body mass. In adults, the differences between migratory and non-migratory sparrows were especially pronounced in the right hippocampus. Juvenile migratory Z. l. gambelii had relatively larger hippocampal volume compared to juvenile non-migratory Z. l. nuttalli. Adult migratory Z. l. gambelii had more neurons in their right hippocampus compared to juveniles but such differences were not found in non-migratory Z. l. nuttalli. Our results suggest that migratory behaviour might be related to enhanced spatial memory and an enlarged hippocampus with more neurons, and that differences in the hippocampus between migratory and non-migratory sparrows might be experience-dependent. Furthermore, for the first time our results suggest that the right hippocampus, which encodes global spatial information, might be involved in migratory behaviour.     

The human hippocampus and spatial and episodic memory

Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.     

The skeleton of early Eocene Cantius, oldest lemuriform primate

A recently discovered partial skeleton of the adapid Cantius trigonodus from the early Eocene Willwood Formation of the Bighorn Basin, Wyoming, documents substantial new information about the anatomy of the oldest lemuriform primates. It is very similar in all features to its descendant, middle Eocene Notharctus, and both exhibit numerous resemblances to certain extant Malagasy lemurs, particularly Lepilemur, Propithecus, Lemur, and Hapalemur griseus. Like these forms, Cantius had relatively long hind limbs and short forelimbs. Forelimb traits (prominent brachialis flange of the humerus, well-developed olecranon process of the ulna, and strong shafts of the ulna and radius) suggest active use of the forelimbs in progression. Specializations in the hind limb (e.g., expanded articular surface of the femoral head, narrow and elevated patellar trochlea and prominent lateral trochlear ridge, posteriorly oriented femoral and tibial condyles, narrow and elongate talus, and hallucal metatarsal with prominent peroneal tubercle) indicate capabilities for leaping and for powerful grasping with an opposable hallux. Cantius was presumably primitive in having a relatively long ischium and much more distal inferior tibial tuberosity than most extant lemurs--traits suggesting that powerful extension of the thigh and flexion at the knee were important in its locomotion and posture. We interpret Cantius as an active arboreal quadruped with a propensity for leaping. The existence of this skeletal structure in one of the oldest primates of modern aspect suggests that it represents the primitive lemuriform morphology.     

The effect of forelimb deafferentation in early postnatal ontogeny on the development of synaptic transmission in the hippocampus]

Hippocampal slices from 15-20-day-old Wistar rats were used to study the development of some features of synaptic transmission in hippocampus and the influence of partial limitation of the sensory inflow in the early ontogeny of this transmission. The dynamics of population spike changes was observed in the CA1 hippocampal field in response to stimulation of Schaffer collaterals. The early ontogenetic limitation of the sensory inflow was accomplished by cutting n. medianus on the 13th day. Between the 15th and 20th days, the dynamics of the population spike amplitude increase in the control and experimental animals was similar, however, the response amplitude of the control rats remained higher than in the experimental animals throughout the whole period of observation. It is suggested that the partial limitation of sensory inflow from a forelimb at the early stages of the ontogeny alters the formation of synaptic transmission in hippocampus.     

Maze-escape learning and memory during rat ontogeny

With the method of a simple automatic rectangular maze the development of escape reaction was studied in albino rats aged 3 weeks to 3 months as well as memory retrieval within 24 h and then after one month. Learning of escape improves sharply between the 3rd and 4th postnatal week, and then, with the exception of week 8, remains approximately on the same level. Memory retrieval up to 24 h is not significantly influenced by age or sex, but is best immediately after learning interval of 10 min and the poorest after 24 h, except the age of 5 weeks, where it is best in 3 and 6 h after learning. One-month retention of maze escape improves during development except in animals trained at the age of 6 weeks in which the level is lower than in all other investigated groups. One-month memory retrieval in animals taught at the age of 4 weeks is influenced by the time of the first retention test with the best values in animals tested for the first time after 3 h and poorest in animals tested after 24 h after learning. Animals trained at 5 weeks had a marginally better result after the one-month retention test in females, perhaps due to the influence of sexual maturation on memory traces. This was not observed in the other age groups. Attention is drawn to the different development of learning and memory of various types of conditioned reactions stemming from the difference in their complexity.     

The premaxilla in Neandertal and early modern children: ontogeny and morphology.

This comparative study of maxillae in Neandertals, Qafzeh, and extant children examines two specific traits: the premaxillary suture (sutura incisiva) and the interincisive sinuses, proposing a new hypothesis about some features of the Neandertal mid-face. Morphologic study of the premaxillary suture at its different borders (i.e. the nasal aspect of the frontal process, nasal and palatal aspects of the palatal process of the maxilla) indicates a persistence of the suture among very young Neandertal children in comparison to the condition in extant ones. This suggests a longer independence of some parts of the premaxilla in Neandertals. To further examine this possibility, CT scans of two Neandertal children were analyzed: Roc de Marsal, estimated to be about 3 years, and Engis 2, estimated to be about 5-6 years. The results are quite different between the fossils. In the older, the premaxillary suture is represented only by a deep groove. In the younger it extends deep to the surface of the nasal process reaching the Parinaud's canal. Synostosis of the premaxillary suture was found to occur later in Neandertal children than in modern ones. Moreover, we observed the existence of two interincisive sinuses in the fossil children, whereas this is rare in modern children (present on only 2% of our sample of 0-6 year-old infants, n = 247).Persistence of an open premaxillary suture represents the potential for an extended period of growth of the Neandertal mid-face. Although no trace of the premaxillary suture remains in adult Neandertals, Neandertals present many features classically considered as consequences of this persistence. The two interincisive sinuses could be a consequence of the labio-lingual diameter of the incisors. The results presented here can be further investigated by additional studies on the cranial sutural system and by precise morphologic observations and CT scans of the mid-face of a larger sample of fossil children.     

Campynemanthe (Campynemaceae): Morphology, microsporogenesis, early ovule ontogeny and relationships

Campynemanthe Baill. consists of three species endemic to New Caledonia. Two species are studied and compared. The tapetum is secretory with 2-nucleate tapetal cells. Microsprogenesis is successive, microspore tetrads are isobilateral and the pollen grains are free and inaperturate or have a weakly defined aperture. Placentation is axile with 3–4 ovules in each of the three locules. Ovules are anatropous and crassinucellate with the micropyle formed by the inner integument alone. The archesporial cell cuts off a parietal cell, which divides to form a parietal tissue. The nucellar epidermis divides periclinally at the nucellar apex to become 2-layered. The megaspore tetrad is T-shaped, in which the micropylar megaspore cells are separated by an oblique wall. The chalazal megaspore enlarges and apparently developes into a Polygonum-type embryo sac, but a mature embryo sac has not been seen. The ripe seeds are pale and non-phytomelaniferous. They have copious endosperm rich in fatty oils. The embryo is minute. These characters and gross morphological similarities support relationship with Campynema Labill., but there are also conspicuous differences. The two genera are considered related. They also closely approach genera of the variable family Melanthiaceae and there are reasons to include them in this family.     

The formation of activity-rest cycles in early ontogeny

The cyclic variations of the motor activity consist of many rhythmic components which appear nonsimultaneously in the ontogenesis. The earliest component is the autogenic periodic motility with the duration about one minute which can be observed in rats during first two-three weeks after the birth. From the second week a new type of cyclic activity appears. It can be qualified as a sleep-wakefulness cycle with the duration about several minutes. It is suggested that this cycle is a true novel rhythm which is able to modulate the earliest more frequent periodicity.     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

The role of hippocampus in long-term memory: dynamic system approach

Several attempts have been made to reconcile a number of concurrent theories on the role of the hippocampus in long-term memory functions. Those attempts fail to explain the basic effects of the theories from the same standpoint. This work is a critical review of the four major theories demonstrating (with the use of mathematical models of attention and memory) that only one of them is capable of reconciling them all by explaining the fundamental effects of each theory in a unified fashion without sacrificing their individual contributions. The key issue here is whether or not a memory trace is ever stored in the hippocampus itself, and there is no reconciliation unless the answer is in the negative.