Jacobs, B. et al. Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb. Cortex 11, 558-571

Laboratory of Quantitative Neuromorphology, Department of Psychology, The Colorado College, 14 E. Cache La Poudre, Colorado Springs, CO 80903, USA.
Cerebral Cortex (Impact Factor: 8.67). 07/2001; 11(6):558-71. DOI: 10.1093/cercor/11.6.558
Source: PubMed


The present study explored differences in dendritic/spine extent across several human cortical regions. Specifically, the basilar dendrites/spines of supragranular pyramidal cells were examined in eight Brodmann's areas (BA) arranged according to Benson's (1993, Behav Neurol 6:75-81) functional hierarchy: primary cortex (somatosensory, BA3-1-2; motor, BA4), unimodal cortex (Wernicke's area, BA22; Broca's area, BA44), heteromodal cortex (supple- mentary motor area, BA6beta; angular gyrus, BA39) and supramodal cortex (superior frontopolar zone, BA10; inferior frontopolar zone, BA11). To capture more general aspects of regional variability, primary and unimodal areas were designated as low integrative regions; heteromodal and supramodal areas were designated as high integrative regions. Tissue was obtained from the left hemisphere of 10 neurologically normal individuals (M(age) = 30 +/- 17 years; five males, five females) and stained with a modified rapid Golgi technique. Ten neurons were sampled from each cortical region (n = 800) and evaluated according to total dendritic length, mean segment length, dendritic segment count, dendritic spine number and dendritic spine density. Despite considerable inter-individual variation, there were significant differences across the eight Brodmann's areas and between the high and low integrative regions for all dendritic and spine measures. Dendritic systems in primary and unimodal regions were consistently less complex than in heteromodal and supramodal areas. The range within these rankings was substantial, with total dendritic length in BA10 being 31% greater than that in BA3-1-2, and dendritic spine number being 69% greater. These findings demonstrate that cortical regions involved in the early stages of processing (e.g. primary sensory areas) generally exhibit less complex dendritic/spine systems than those regions involved in the later stages of information processing (e.g. prefrontal cortex). This dendritic progression appears to reflect significant differences in the nature of cortical processing, with spine-dense neurons at hierarchically higher association levels integrating a broader range of synaptic input than those at lower cortical levels.

Download full-text


Available from: Bob Jacobs,
  • Source
    • "Increasing dendritic complexity and density is associated with hierarchical computational capacity of cortical structures(Jacobs et al., 2001). In white matter, orientation dispersion captures the bending and fanning of fibres, important for determining anatomical connectivity(Kaden, Knosche, & Anwander, 2007), while in grey matter it captures sprawling dendritic processes, providing a more accurate measure of grey matter complexity(Zhang, Schneider, Wheeler-Kingshott, & Alexander, 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Discrete yet overlapping frontal-striatal circuits mediate broadly dissociable cognitive and behavioural processes. Using a recently developed multi-echo resting-state functional MRI sequence with greatly enhanced signal compared to noise ratios, we map frontal cortical functional projections to the striatum and striatal projections through the direct and indirect basal ganglia circuit. We demonstrate distinct limbic (ventromedial prefrontal regions, ventral striatum, ventral tegmental area), motor (supplementary motor areas, putamen, substantia nigra) and cognitive (lateral prefrontal and caudate) functional connectivity. We confirm the functional nature of the cortico-striatal connections, demonstrating correlates of well-established goal directed behaviour (involving medial orbitofrontal cortex and ventral striatum), probabilistic reversal learning (lateral orbitofrontal cortex and ventral striatum) and attentional shifting (dorsolateral prefrontal cortex and ventral striatum) while assessing habitual model-free (supplementary motor area and putamen) behaviours on an exploratory basis. We further use neurite orientation and dispersion density imaging (NODDI) to show that more goal-directed model-based learning is also associated with higher medial orbitofrontal cortex neurite density and habitual model-free learning implicates neurite complexity in the putamen. This data highlights similarities between a computational account of model-free learning and conventional measures of habit learning. We highlight the intrinsic functional and structural architecture of parallel systems of behavioural control.
    Cortex 11/2015; DOI:10.1016/j.cortex.2015.11.004 · 5.13 Impact Factor
    • "In the most of mammalian forebrain structures, pyramidal neurons are found and have been associated with sophisticated cognitive functions. Although pyramidal cells have common features , differences in neuron structure have been described among different regions of the brain and different species (Elston 2000; Jacobs et al. 2001; Ballesteros-Yáñez et al. 2006; Benavides-Piccione et al. 2006; Elston et al. 2011; Oga et al. 2013; Elston & Manger 2014), and the differences in their structure are thought to underpin functional differences (see Elston 2003; Jacobs & Scheibel 2002; Spruston 2008; Elston & Fujita 2014 for reviews). We previously reported strain-specific differences between LEW and F344 rats in different brain areas including the hippocampus (Ballesteros-Yanez et al. 2007a; Ballesteros-Yanez et al. 2008; Miguens et al. 2015). "
    [Show abstract] [Hide abstract]
    ABSTRACT: We previously showed that cocaine self-administration increases spine density in CA1 hippocampal neurons in Lewis (LEW) but not in Fischer 344 (F344) rats. Dendritic spine morphology is intimately related to its function. Thus, we conducted a 3D morphological analysis of CA1 dendrites and dendritic spines in these two strains of rats. Strain-specific differences were observed prior to cocaine self-administration: LEW rats had significantly larger dendritic diameters but lower spine density than the F344 strain. After cocaine self-administration, proximal dendritic volume, dendritic surface area and spine density were increased in LEW rats, where a higher percentage of larger spines were also observed. In addition, we found a strong positive correlation between dendritic volume and spine morphology, and a moderate correlation between dendritic volume and spine density in cocaine self-administered LEW rats, an effect that was not evident in any other condition. By contrast, after cocaine self-administration, F334 rats showed decreased spine head volumes. Our findings suggest that genetic differences could play a key role in the structural plasticity induced by cocaine in CA1 pyramidal neurons. These cocaine-induced alterations could be related to differences in the memory processing of drug reward cues that could potentially explain differential individual vulnerability to cocaine addiction. © 2015 Society for the Study of Addiction.
    Addiction Biology 09/2015; DOI:10.1111/adb.12294 · 5.36 Impact Factor
  • Source
    • "We addressed this gap in our understanding of human brain organization using intracellular dye loading of individual excitatory neurons in acute, living brain slices of human temporal cortex to avoid potential effects of postmortem delays on cellular morphology. The dimensions of our living brain slices (350 µm) exceed typical slice dimensions for conventional Golgi-Cox stainings on human brain samples (100–200 µm, (Jacobs et al. 2001; Petanjek et al. 2008; Zeba et al. 2008)) and truncation artifacts due to sectioning are therefore relatively small (van Pelt et al. 2014). Using this approach, we tested the hypothesis that total dendritic length of human Layer (L)2 and L3 pyramidal neurons (including basal, apical oblique dendrites, main apical trunk, and distal tuft) are distinct from mouse and macaque pyramidal neurons. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The size and shape of dendrites and axons are strong determinants of neuronal information processing. Our knowledge on neuronal structure and function is primarily based on brains of laboratory animals. Whether it translates to human is not known since quantitative data on "full" human neuronal morphologies are lacking. Here, we obtained human brain tissue during resection surgery and reconstructed basal and apical dendrites and axons of individual neurons across all cortical layers in temporal cortex (Brodmann area 21). Importantly, morphologies did not correlate to etiology, disease severity, or disease duration. Next, we show that human L(ayer) 2 and L3 pyramidal neurons have 3-fold larger dendritic length and increased branch complexity with longer segments compared with temporal cortex neurons from macaque and mouse. Unsupervised cluster analysis classified 88% of human L2 and L3 neurons into human-specific clusters distinct from mouse and macaque neurons. Computational modeling of passive electrical properties to assess the functional impact of large dendrites indicates stronger signal attenuation of electrical inputs compared with mouse. We thus provide a quantitative analysis of "full" human neuron morphologies and present direct evidence that human neurons are not "scaled-up" versions of rodent or macaque neurons, but have unique structural and functional properties. © The Author 2015. Published by Oxford University Press.
    Cerebral Cortex 08/2015; DOI:10.1093/cercor/bhv188 · 8.67 Impact Factor
Show more