Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.

Jacobs, Lucia F.; Gaulin, Steven J. C.; Sherry, David F.; Hoffman, Gloria E.

doi:10.1073/pnas.87.16.6349

Cited by 334 publications

(230 citation statements)

References 47 publications

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“…Thus, they were showing evidence of greater stimulus competition than females from the same age periods. Such observation seems at consonance with evidence showing greater hippocampal development in males from some rodent species (e.g., Jacobs, 1996;Jacobs, Gaulin, Sherry, & Hoffman, 1990). Although quite a speculative idea at present, the sex differences we have documented may eventually provide further support for the view of the hippocampus as the neuroanatomical structure underlying stimulus competition in the rat brain.…”

Section: Discussionsupporting

confidence: 88%

Contextual fear conditioning differs for infant, adolescent, and adult rats

Esmoris-Arranz¹,

Méndez²,

Spear³

2008

Behavioural Processes

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Contextual fear conditioning was tested in infant, adolescent, and adult rats in terms of Pavlovian conditioned suppression. When a discrete auditory conditioned stimulus (CS) was paired with footshock (unconditioned stimulus, US) within the largely olfactory context, infants and adolescents conditioned to the context with substantial effectiveness but adult rats did not. When unpaired presentations of the CS and US occurred within the context, contextual fear conditioning was strong for adults, weak for infants, but about as strong for adolescents as when pairings of CS and US occurred in the context. Nonreinforced presentations of either the CS or context markedly reduced contextual fear conditioning in infants, but, in adolescents, CS extinction had no effect on contextual fear conditioning, although context extinction significantly reduced it. Neither CS extinction nor context extinction affected responding to the CS-context compound in infants, suggesting striking discrimination between the compound and its components. Female adolescents showed the same lack of effect of component extinction on response to the compound as infants, but CS extinction reduced responding to the compound in adolescent males, a sex difference seen also in adults. Theoretical implications are discussed for the development of perceptual-cognitive processing and hippocampus role. Keywordscontextual fear conditioning; fear extinction; learning; olfactory context; hippocampus; ontogeny Contextual fear conditioning has received a lot of attention from behavioral neuroscientists during the last decade (e.g., Anagnostaras, Gale, & Fanselow, 2001;Fanselow & Poulos, 2004;Phillips & LeDoux, 1992). The purpose of this report is to assess the effectiveness of contextual fear conditioning experiments by rats at each of three disparate periods of ontogeny: late infancy, adolescence and early adulthood. The ontogeny of contextual fear conditioning is of interest because --in relation to conditioning of other events within the context--it can Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. provide a window to the ontogeny of encoding and memory organization (e.g., Brasser & Spear, 2004;Lariviere, Chen, & Spear, 1990), and because it has been used as a marker for the development of brain function important for memory (e.g., Pugh & Rudy, 1996;Rudy & Morledge, 1994). NIH Public AccessSeveral experiments led to the conclusion that acquisition of an aversion to a particular context paired with footshock is less effective in rats during late infancy (postnatal days 17-20, P17-20) than in weaned juvenile ...

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Section: Discussionsupporting

confidence: 88%

Contextual fear conditioning differs for infant, adolescent, and adult rats

Esmoris-Arranz¹,

Méndez²,

Spear³

2008

Behavioural Processes

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“…Vole species with different home ranges and habitats vary with respect to hippocampal size and microstructure. This correlates with spatial behaviour in the field and in the laboratory [19,36]. In natural mouse populations similar aptations occur [5].…”

Section: Introductionsupporting

confidence: 52%

Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice

Lewejohann

Skryabin

Sachser

et al. 2004

Behavioural Brain Research

139

102

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BC1 RNA is a small non-messenger RNA common in dendritic microdomains of neurons in rodents. In order to investigate its possible role in learning and behaviour, we compared controls and knockout mice from three independent founder lines established from separate embryonic stem cells. Mutant mice were healthy with normal brain morphology and appeared to have no neurological deficits. A series of tests for exploration and spatial memory was carried out in three different laboratories. The tests were chosen as to ensure that different aspects of spatial memory and exploration could be separated and that possible effects of confounding variables could be minimised. Exploration was studied in a barrier test, in an open-field test, and in an elevated plus-maze test. Spatial memory was investigated in a Barnes maze and in a Morris water maze (memory for a single location), in a multiple T-maze and in a complex alley maze (route learning), and in a radial maze (working memory). In addition to these laboratory tasks, exploratory behaviour and spatial memory were assessed under semi-naturalistic conditions in a large outdoor pen. The combined results indicate that BC1 RNA-deficient animals show behavioural changes best interpreted in terms of reduced exploration and increased anxiety. In contrast, spatial memory was not affected. In the outdoor pen, the survival rates of BC1-depleted mice were lower than in controls. Thus, we conclude that the neuron-specific non-messenger BC1 RNA contributes to the aptive modulation of behaviour.

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“…This work began with the demonstration of gender differences in spatial learning in species in which there are gender differences in natural range size, that is, if males and females of a given species of voles use space differently, this is mirrored by differences in their spatial maze performance when they are brought into the laboratory (Gaulin and Fitzgerald, 1986;. The critical next step was taken by Jacobs et al (1990). who demonstrated that there are gender differences in hippocampal size in a species of voles showing habitat range and spatial learning dimorphism.…”

Section: The Special Nature O F Spatialmentioning

confidence: 99%

The hippocampus and space revisited

1991

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The hippocampal formation has long been the focus of intense interest among neuroscientists. The discovery by Scoville and Milner (1957) that the mesial temporal lobe, including the hippocampal formation, played a central role in memory function in humans can be said to have started the modern era of research on this brain system. There followed two decades of animal research aimed at creating experimental models of the memory defects observed in humans, including my dissertation research, which met with scant success (Nadel, 1968). Indeed, when John O'Keefe and I started considering the hippocampus and its possible role in spatial mapping several years later, one of our greatest challenges was to analyze the extant lesion literature in terms of this theory with the minimum amount of special pleading. There were already several hundred such studies, varying extensively in terms of exact size and regional location of the lesion, the means by which the lesion had been created, the kind of animal used, the nature of the task, the kind of motivation employed, and so on. Yet, it was our feeling in 1976, when we terminated the review of the lesion literature, which was ultimately published in The Hippocumpiis CIS a Cognitive Map (O'Keefe and Nadel, 1978), that the spatial hypothesis successfully handled the vast preponderance of these lesion studies as well as what was then known about the physiology of the hippocampal formation.In the years following publication of the book, most published lesion studies were concerned in some way with the spatial map hypothesis; most often, comparisons with rival hypotheses were involved. This was a frustrating period because, although many thought they were testing our ideas, too frequently the major themes we hoped to stress were misconstrued. In this article I dig back into the book we published in 1978 and reiterate some of the themes that were important to us then, and remain so now. By so doing, 1 hope to bring out some of the reasons why we thought, and continue to think, that space is so special as to warrant a structure as compelling as the hippocampal formation.I will concentrate on three major issues. First, I will discuss at some length the fact that our theory was about a ~p a t i a l memory system, not simply a "spatial" system. Second, Iwill discuss our assumption that the spatial memory system we allocated to the hippocampus was but one of many spatial systems, and that the role of these various systems can best be understood if one takes into consideration an animal's behavior in its natural habitat. Third, I will briefly discuss our view that in the human hippocampus, at least in the left hemisphere, the mapping system represents something more abstract than physical space.Before turning to these substantive points, however, a brief digression into methods and first principles is in order. Some years before the book was published, O'Keefe and I published a paper (Nadel and O'Keefe, 1974) in which we presented some of the reasons for hypothesizing that the hippocamp...

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Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.

Cited by 334 publications

References 47 publications

Contextual fear conditioning differs for infant, adolescent, and adult rats

Contextual fear conditioning differs for infant, adolescent, and adult rats

Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice

The hippocampus and space revisited

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