Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison

Roth, Timothy C.; Pravosudov, Vladimir V.

doi:10.1098/rspb.2008.1184

Cited by 128 publications

(223 citation statements)

References 24 publications

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“…More importantly, after the brain tissue is extracted from the animal, it is generally post-fixed in a formalin solution for a period ranging from a day to several weeks (e.g. Pravosudov & Clayton 2002;LaDage et al 2009b;Roth & Pravosudov 2009). This is yet another very important point where considerable tissue shrinkage may occur (Quester & Schroder 1997 and references therein; T. C. Roth, L. D. LaDage & V. V. Pravosudov, unpublished data).…”

Section: Problems With the Compatibility Of Data Across Studiesmentioning

confidence: 99%

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Roth

Brodin

Smulders

et al. 2010

Phil. Trans. R. Soc. B

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A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.

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Section: Problems With the Compatibility Of Data Across Studiesmentioning

confidence: 99%

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Roth

Brodin

Smulders

et al. 2010

Phil. Trans. R. Soc. B

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“…A number of hypotheses have been generated to explain how selection may have driven changes in brain size (Francis, 1995;Barton and Harvey, 2000; de Winter and Oxnard, 2001;Hutcheon et al, 2002; Byrne and Corp, 2004;Lefebvre et al, 2004;Marino, 2005;Sol et al, 2005;Lefebvre and Sol, 2008;Rehkämper et al, 2008;Sol et al, 2008; Chittka and Niven, 2009;Roth and Pravosudov, 2009). Most, if not all, of these hypotheses suggest that selection is acting on behavior [e.g.…”

Section: Discussionmentioning

confidence: 99%

Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model of brain evolution

Kolb

Rezende

Holness

et al. 2013

Journal of Experimental Biology

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SUMMARYIncreased brain size, relative to body mass, is a primary characteristic distinguishing the mammalian lineage. This greater encephalization has come with increased behavioral complexity and, accordingly, it has been suggested that selection on behavioral traits has been a significant factor leading to the evolution of larger whole-brain mass. In addition, brains may evolve in a mosaic fashion, with functional components having some freedom to evolve independently from other components, irrespective of, or in addition to, changes in size of the whole brain. We tested whether long-term selective breeding for high voluntary wheel running in laboratory house mice results in changes in brain size, and whether those changes have occurred in a concerted or mosaic fashion. We measured wet and dry brain mass via dissections and brain volume with ex vivo magnetic resonance imaging of brains that distinguished the caudate-putamen, hippocampus, midbrain, cerebellum and forebrain. Adjusting for body mass as a covariate, mice from the four replicate high-runner (HR) lines had statistically larger non-cerebellar wet and dry brain masses than those from four non-selected control lines, with no differences in cerebellum wet or dry mass or volume. Moreover, the midbrain volume in HR mice was ~13% larger (P<0.05), while volumes of the caudate-putamen, hippocampus, cerebellum and forebrain did not differ statistically between HR and control lines. We hypothesize that the enlarged midbrain of HR mice is related to altered neurophysiological function in their dopaminergic system. To our knowledge, this is the first example in which selection for a particular mammalian behavior has been shown to result in a change in size of a specific brain region.Key words: activity, allometry, cerebellum, dopamine, exercise behavior, locomotion, motor control. convergences within primates, spatio-sensory convergences within insectivores). Similar evidence for mosaic evolution in the avian brain has also been found and correlated to functional differences in the enlarged brain regions (Iwaniuk et al., 2006). Cellular changes have also been observed with increased brain size. As brain volume increases, axon diameters and the fraction of myelinated axons increase, thereby reducing the delay in neural signaling between more distant regions (Wang et al., 2008). Moreover, different cellular scaling rules apply across different mammalian orders (Herculano-Houzel, 2010). For example, in rodents, neuronal cell size increases with brain size, such that neuronal density is lower in larger-brained species (albeit with a greater absolute number of neurons) (Herculano-Houzel et al., 2006). Conversely, in primates, neuronal cell size is constant and neuron density is constant, such that total neuron number is much greater with increasing brain size (Herculano-Houzel et al., 2007). Therefore, an increase in the size of a brain region could be the product of a variety of cellular changes (e.g. neuron number, neuron density, glial density, gray-to-white matte...

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“…At the time of year when most items are being stored, the HF of black-capped chickadees is larger (Smulders et al 1995), containing more cells and incorporating more newly generated neurons (Barnea & Nottebohm 1994) than at other times of the year (see also Roth et al 2010;Sherry & Hoshooley 2010). Similarly, populations of black-capped chickadees that hoard more food have a larger hippocampus with more neurons than populations that hoard less food Roth & Pravosudov 2009). These correlations should be treated with caution, however, as demand for high capacity may covary with a demand for high spatial resolution (although it may not; see below), such that it is difficult to assign the differences in neuroanatomy to one or the other of the two aspects of spatial memory (or indeed any other correlating variables).…”

Section: Using Ecology To Predict Specific Memory Adaptationsmentioning

confidence: 99%

Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals

Smulders

Gould

Leaver

2010

Phil. Trans. R. Soc. B

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Understanding the survival value of behaviour does not tell us how the mechanisms that control this behaviour work. Nevertheless, understanding survival value can guide the study of these mechanisms. In this paper, we apply this principle to understanding the cognitive mechanisms that support cache retrieval in scatter-hoarding animals. We believe it is too simplistic to predict that all scatter-hoarding animals will outperform non-hoarding animals on all tests of spatial memory. Instead, we argue that we should look at the detailed ecology and natural history of each species. This understanding of natural history then allows us to make predictions about which aspects of spatial memory should be better in which species. We use the natural hoarding behaviour of the three best-studied groups of scatter-hoarding animals to make predictions about three aspects of their spatial memory: duration, capacity and spatial resolution, and we test these predictions against the existing literature. Having laid out how ecology and natural history can be used to predict detailed cognitive abilities, we then suggest using this approach to guide the study of the neural basis of these abilities. We believe that this complementary approach will reveal aspects of memory processing that would otherwise be difficult to discover.

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Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison

Cited by 128 publications

References 24 publications

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model of brain evolution

Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals

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