Astrocytes in Human Evolution

Alfredo Pereira Jr

Thursday, 30 Aug 2007 21:14 UTC

Thanks to Malcolm Dean for calling my attention to the paragraph below, from a new paper by D. Premack

”...specialized neuroglial cells called astrocytes (which make up nearly half the cells in the human brain) must be present for synapses to form; these cells secrete a protein called thrombospondin that triggers synapse formation. Preuss and associates then found that human brains produce up to six times as much thrombospondin messenger RNA than do either chimps or macaques. Moreover, the areas found to have enhanced thrombospondin expression have larger neuropil space and thus more room for synaptic connections. Virtually all the newly discovered human singularities are located in areas associated with either complex social cognition [theory of mind (TOM)] or language. But the reorganization of the human brain has not been without cost. In addition to advancing language and TOM, it brought about neurodegenerative disease: schizophrenia, autism, Alzheimer’s, etc. These diseases are as unique to humans as is advanced cognitive function.”

Reference:

David Premack (2007) Human and animal cognition: Continuity and discontinuity. Published online before print August 23, 2007, 10.1073/pnas.0706147104
PNAS | August 28, 2007 | vol. 104 | no. 35 | 13861-13867

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    • Dear Alfredo,

      Please could you help me out here:

      Everyone knows that the symptoms of Alzheimer’s disease are the result of neurodegeneration.

      But that schizophrenia and autism are also neurodegenerative ‘diseases’ – as stated in the above quote – is a new one on me.

      Or is it just now accepted that autism and schizophrenia must somehow be neurodegenerative diseases?

      I’m afraid I haven’t read the article because I can’t afford to start buying articles online.

      With best wishes,
      Michael

    • Dear Michael:

      This publication is free, just click on the link in my first message (“new paper by D. Premack”).

      I do not have a good answer for your question.
      I will wait for a help from other members of the group.

      My suggestion is that the author called “neurodegenerative” to brain illnesses that begin after the first years of life.

      Best Regards

      Alfredo

    • Hi Alfredo,

      When I click on the link, and then click on ‘Full Text’, I read the following: “This item requires a subscription to Proceedings of the National Academy of Sciences Online.” Alternatively, I’m invited to purchase short-term access the article.

      Access may be free for you because your university pays for the subscription to National Academy of Sciences, or something like that.

      I wouldn’t be inclined to say that autism or schizophrenia are ‘brain illnesses’. Obviously they are, respectively, developmental disorders and mental disorders; they both can be profoundly pathological; and there is no question that understanding the nature of these disorders requires a better understanding of the human nervous system than we currently have.

      But equally, they both seem occasionally to be involved in genius.

      Moreover, Hans Asperger himself wrote: “The autistic personality is an extreme variant of masculine intelligence, of masculine character.” So if we simply say that autism is a brain illness, then it’s a bit like saying that extreme masculinity is a brain illness. (No doubt some would say that it is indeed.)

      Best wishes,
      Michael

    • This content has been removed by the forum moderators.

    • Dear All:

      Nature Neuroscience (10, 1349, 2007)released a new number focusing on glia. Below I pasted some parts of the Editorial written by Sandra Aamodt.

      Best Regards,

      Alfredo

      “A decade ago, glia were the neglected stepchildren of neuroscience. Although glia outnumber neurons by about ten to 1 in the adult human brain, providing support for neurons has traditionally been viewed as their primary function. Glial biology has come into its own recently, as researchers have shown that glia are critical for the development of the nervous system and have key roles in various neurodegenerative disorders. Glia regulate brain vasculature and the blood-brain barrier, modulating ischemia and migraines. Moreover, they are important in the repair of neurons after injury and also contribute to neuropathology in neurodegenerative diseases. In this issue, we present a focus on glia and disease, which highlights recent efforts in some of these areas and discusses how advances in understanding glial biology may lead to new treatments.
      Multiple sclerosis is caused by the malfunction of glia, specifically by the failure of remyelination by oligodendrocytes. ...
      Glia are also important in dominantly inherited neurodegenerative diseases, including amyotrophic lateral sclerosis, spinocerebellar ataxia, Parkinson’s disease and Huntington’s disease. ...
      Neuropathic pain is triggered by a normally innocuous stimulus or by no stimulus at all. Glia, immune cells and neurons interact to produce neuropathic pain, explain Joachim Scholz and Clifford Woolf in their review. They describe neuropathic pain as a neuroimmune disorder, involving activation of Schwann cells, microglia and astrocytes in a complex temporal and spatial pattern. Blocking the signaling pathways between neurons and non-neuronal cells may offer new ways to prevent or treat this disorder, but a key challenge for the future will be to differentiate the healthy aspects of pathways that are activated in response to pain-inducing stimuli from those that produce neuropathology.
      Local control of blood flow in the brain is important for matching neural activity to the brain’s local supply of oxygen and glucose, a process that provides the basis for functional imaging techniques. In their review, Costantino Iadecola and Maiken Nedergaard discuss the mechanisms by which astrocytes regulate microvasculature. Changes in intracellular calcium in astrocytic endfeet regulate vascular tone in the arterioles that they contact. Because synaptic activity is not the only process that influences astrocytic calcium levels and because astrocytes integrate synaptic activity over long time scales, the authors caution that the interpretation of functional brain imaging signals may need to be reevaluated. These results also raise the speculation that astrocytes may participate in cerebrovascular disease.
      Astrocytes clearly contribute to one form of cerebrovascular disorder, brain ischemia, which is often caused by stroke. David Rossi, James Brady and Claudia Mohr review the mechanisms by which astrocytes damage and protect neurons that have lost their blood supply. Astrocytic glycogen stores can provide energy to deprived neurons, but can also increase brain damage as a result of lactic acidosis. Release of neurotransmitters such as glutamate from astrocytes can contribute to ischemic brain damage. Because astrocytes are coupled into networks by gap junctions, they are also important in the spread of stroke-induced damage to bystander neurons surrounding the initial injury. Once brain ischemia has begun, it is difficult to deliver drugs to the affected areas, so the authors concentrate on therapeutic agents that could be given to high-risk patients to reduce the damage caused by stroke….”

    • A PubMed search on PG Haydon (one of the leading researchers on astrocytes):

      1: J Neurosci. 2007 Jun 13;27(24):6473-7.

      Synaptic islands defined by the territory of a single astrocyte.

      Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG.

      Silvio Conte Center for Integration at the Tripartite Synapse, Department of
      Neuroscience, University of Pennsylvania School of Medicine, Philadelphia,
      Pennsylvania 19104, USA.

      In the mammalian brain, astrocytes modulate neuronal function, in part, by
      synchronizing neuronal firing and coordinating synaptic networks. Little,
      however, is known about how this is accomplished from a structural standpoint. To
      investigate the structural basis of astrocyte-mediated neuronal synchrony and
      synaptic coordination, the three-dimensional relationships between cortical
      astrocytes and neurons was investigated. Using a transgenic and viral approach to
      label astrocytes with enhanced green fluorescent protein, we performed a
      three-dimensional reconstruction of astrocytes from tissue sections or live
      animals in vivo. We found that cortical astrocytes occupy nonoverlapping
      territories similar to those described in the hippocampus. Using
      immunofluorescence labeling of neuronal somata, a single astrocyte enwraps on
      average four neuronal somata with an upper limit of eight. Single-neuron
      dye-fills allowed us to estimate that one astrocyte contacts 300-600 neuronal
      dendrites. Together with the recent findings showing that glial Ca2+ signaling is
      restricted to individual astrocytes in vivo, and that Ca2+ signaling leads to
      gliotransmission, we propose the concept of functional islands of synapses in
      which groups of synapses confined within the boundaries of an individual
      astrocyte are modulated by the gliotransmitter environment controlled by that
      astrocyte. Our description offers a new structurally based conceptual framework
      to evaluate functional data involving interactions between neurons and astrocytes
      in the mammalian brain.

      PMID: 17567808 [PubMed – indexed for MEDLINE]

      Related Links

      Differential neurite growth on astrocyte substrates: interspecies facilitation in
      green fluorescent protein-transfected rat and human neurons. [Neuroscience. 2000]
      PMID:10658640

      Properties of synaptically evoked astrocyte calcium signal reveal synaptic
      information processing by astrocytes. [J Neurosci. 2005] PMID:15745945

      Astrocyte control of synaptic transmission and neurovascular coupling. [Physiol
      Rev. 2006] PMID:16816144

      Selective stimulation of astrocyte calcium in situ does not affect neuronal
      excitatory synaptic activity. [Neuron. 2007] PMID:17521573

      Astrocyte-derived estrogen enhances synapse formation and synaptic transmission
      between cultured neonatal rat cortical neurons. [Neuroscience. 2007]
      PMID:17184929

      2: J Neurosci. 2007 Oct 3;27(40):10674-84.

      Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after
      status epilepticus.

      Ding S, Fellin T, Zhu Y, Lee SY, Auberson YP, Meaney DF, Coulter DA, Carmignoto
      G, Haydon PG.

      Silvio Conte Center for Integration at the Tripartite Synapse, Department of
      Neuroscience, University of Pennsylvania School of Medicine, Philadelphia,
      Pennsylvania 19104, USA.

      Status epilepticus (SE), an unremitting seizure, is known to cause a variety of
      traumatic responses including delayed neuronal death and later cognitive decline.
      Although excitotoxicity has been implicated in this delayed process, the cellular
      mechanisms are unclear. Because our previous brain slice studies have shown that
      chemically induced epileptiform activity can lead to elevated astrocytic Ca2+
      signaling and because these signals are able to induce the release of the
      excitotoxic transmitter glutamate from these glia, we asked whether astrocytes
      are activated during status epilepticus and whether they contribute to delayed
      neuronal death in vivo. Using two-photon microscopy in vivo, we show that status
      epilepticus enhances astrocytic Ca2+ signals for 3 d and that the period of
      elevated glial Ca2+ signaling is correlated with the period of delayed neuronal
      death. To ask whether astrocytes contribute to delayed neuronal death, we first
      administered antagonists which inhibit gliotransmission: MPEP
      [2-methyl-6-(phenylethynyl)pyridine], a metabotropic glutamate receptor 5
      antagonist that blocks astrocytic Ca2+ signals in vivo, and ifenprodil, an NMDA
      receptor antagonist that reduces the actions of glial-derived glutamate.
      Administration of these antagonists after SE provided significant neuronal
      protection raising the potential for a glial contribution to neuronal death. To
      test this glial hypothesis directly, we loaded Ca2+ chelators selectively into
      astrocytes after status epilepticus. We demonstrate that the selective
      attenuation of glial Ca2+ signals leads to neuronal protection. These
      observations support neurotoxic roles for astrocytic gliotransmission in
      pathological conditions and identify this process as a novel therapeutic target.

      PMID: 17913901 [PubMed – in process]

      Related Links

      Role of neuronal NR2B subunit-containing NMDA receptor-mediated Ca2+ influx and
      astrocytic activation in cultured mouse cortical neurons and astrocytes.
      [Synapse. 2006] PMID:16235228

      mGluR5 antagonists 2-methyl-6-(phenylethynyl)pyridine and
      (E)-2-methyl-6
      (2-phenylethenyl)-pyridine reduce traumatic neuronal injury in
      vitro and in vivo by antagonizing N-methyl-D-aspartate receptors. [J Pharmacol
      Exp Ther. 2001] PMID:11123360

      Glutamate release from astrocytes as a non-synaptic mechanism for neuronal
      synchronization in the hippocampus. [J Physiol Paris. 2006] PMID:16646155

      Protective mechanisms of adenosine in neurons and glial cells. [Ann N Y Acad Sci.
      1997] PMID:9369970

      Hippocampal astrocytes in situ respond to glutamate released from synaptic
      terminals. [J Neurosci. 1996] PMID:8756437

      3: ScientificWorldJournal. 2007 Nov 2;7:89-97.

      Astrocytes control neuronal excitability in the nucleus accumbens.

      Fellin T, D’Ascenzo M, Haydon PG.

      Department of Neuroscience, University of Pennsylvania School of Medicine,
      Philadelphia, PA 19104, USA. tfellin@mail.med.upenn.edu

      Though accumulating evidence shows that the metabotropic glutamate receptor 5
      (mGluR5) mediates some of the actions of extracellular glutamate after cocaine
      use, the cellular events underlying this action are poorly understood. In this
      review, we will discuss recent results showing that mGluR5 receptors are key
      regulators of astrocyte activity. Synaptic release of glutamate activates mGluR5
      expressed in perisynaptic astrocytes and generates intense Ca2+ signaling in
      these cells. Ca2+ oscillations, in turn, trigger the release from astrocytes of
      the gliotransmitter glutamate, which modulates neuronal excitability by
      activating NMDA receptors. By integrating these results with the most recent
      evidence demonstrating the importance of astrocytes in the regulation of neuronal
      excitability, we propose that astrocytes are involved in mediating some of the
      mGluR5-dependent drug-induced behaviors.

      PMID: 17982581 [PubMed – in process]

      Related Links

      mGluR5 stimulates gliotransmission in the nucleus accumbens. [Proc Natl Acad Sci
      U S A. 2007] PMID:17259307

      Metabotropic glutamate receptor mGluR5 subcellular distribution and developmental
      expression in hypothalamus. [J Comp Neurol. 1995] PMID:8576426

      The metabotropic glutamate receptor mGluR5 induces calcium oscillations in
      cultured astrocytes via protein kinase C phosphorylation. [J Neurochem. 1997]
      PMID:9326275

      Bidirectional astrocyte-neuron communication: the many roles of glutamate and
      ATP. [Novartis Found Symp. 2006] PMID:16805432

      A novel Ca2+-independent signaling pathway to extracellular signal-regulated
      protein kinase by coactivation of NMDA receptors and metabotropic glutamate
      receptor 5 in neurons. [J Neurosci. 2004] PMID:15574735

    • Nature Neuroscience 11, 379 – 380 (2008)
      doi:10.1038/nn0408-379
      Glia get excited

      A new study shows that a subset of the glia that express the
      proteoglycan NG2 can fire action potentials, contradicting the dogma
      that only neurons are excitable in the brain. These glia receive
      excitatory and inhibitory synaptic input, are selectively vulnerable
      to ischemia and are present into adulthood, though their function
      remains mysterious.

    • This is an exciting paper (of course, I’m biased!) Since these cells are technically not fully-differentiated, it will be interesting to see what role the activity plays in causing these cells to become mature oligodendrocytes, or something else…

    • Another publication (with informative Abstract below) that I missed before Malcolm Dean called my attention:

      http://jp.physoc.org/cgi/reprint/559/1/3
      J Physiol Volume 559(1):3-15, August 15, 2004
      DOI: 10.1113/jphysiol.2004.063214
      Neurone-to-astrocyte signalling in the brain represents a distinct
      multifunctional unit
      Tommaso Fellin and Giorgio Carmignoto

      Astrocytes can respond to neurotransmitters released at the synapse by
      generating elevations in intracellular Ca2+ concentration ([Ca2+]i)
      and releasing glutamate that signals back to neurones. This discovery
      opens new perspectives for the possible participation of these glial
      cells in actual information processing by the brain and raises the
      hypothesis that astrocyte activation by neuronal signals plays a key
      role in distinct, functional events. Depending on the level of
      neuronal activity, the [Ca2+]i response that is activated by
      neurotransmitters can either remain restricted to an astrocytic
      process or it can propagate as an intracellular [Ca2+]i wave to other
      astrocytic processes in contact with different neurones, astrocytes,
      microglia or endothelial cells of cerebral arterioles. Glutamate
      release triggered by the [Ca2+]i rise at the astrocytic process
      represents a feedback, short-distance signal that affects synaptic
      transmission locally. The release of glutamate as well as of other
      compounds far away from the site of initial activation represents a
      feedforward, long-distance signal that can be involved in the
      regulation of distinct processes. For instance, through the release of
      vasoactive molecules from the astrocytic processes in contact with
      cerebral arterioles, the neurone–astrocyte–endothelial cell signalling
      pathway plays a pivotal role in the neuronal control of vascular tone.
      In this article we will review recent results that should persuade us
      to reshape our current thinking on the roles of astroglial cells in
      the brain. We propose that neurones and astrocytes represent an
      integral unit that has a distinctive role in different fundamental
      events in brain function. Furthermore, while recent findings provide
      important evidences for the vesicular hypothesis of glutamate release,
      we discuss also the proposals for a possible physiological role of
      hemichannels and purinergic P2X7 receptors in glutamate release from
      astrocytes. A full clarification of the functional significance of the
      bidirectional communication that astrocytes establish with neurones as
      well as with other brain cells represents one of the most intriguing
      challenges in neurobiological research at the moment and should fuel
      stimulating debates in years to come.

    • Another Abstract that the Dean sent me:

      http://www3.interscience.wiley.com/journal/117934900/abstract
      Glia 56(7):699 – 708, 2008
      DOI 10.1002/glia.20642
      All vertebrates started out with a glial blood-brain barrier 4-500
      million years ago
      Magnus Bundgaard, N. Joan Abbott

      All extant vertebrates have a blood-brain barrier (BBB), a specialized
      layer of cells that controls molecular traffic between blood and
      brain, and contributes to the regulation (homeostasis) of the brain
      microenvironment. Such homeostasis is critical for the stable function
      of synapses and neural networks. The barrier is formed by vascular
      endothelial cells in most groups, but by perivascular glial cells
      (astrocytes) in elasmobranch fish (sharks, skates, and rays). It has
      been unclear which is the ancestral form, but this information is
      important, as it could offer insights into the roles of the
      endothelium and perivascular glia in the modern mammalian BBB. We have
      used electron microscopic techniques to examine three further ancient
      fish groups, with intravascular horseradish peroxidase as permeability
      tracer. We find that in bichir and lungfish the barrier is formed by
      brain endothelial cells, while in sturgeon it is formed by a complex
      perivascular glial sheath, but with no detectable tight junctions.
      From their BBB pattern, and position on the vertebrate family tree, we
      conclude that the ancestral vertebrate had a glial BBB. This means
      that an endothelial barrier would have arisen independently several
      times during evolution, and implies that an endothelial barrier gave
      strong selective advantage. The selective advantage may derive partly
      from greater separation of function between endothelium and astrocytic
      glia. There are important implications for the development,
      physiology, and pathology of the mammalian BBB, and for the roles of
      endothelium and glia in CNS barrier layers.

      Keywords: fish • evolution • brain blood vessels • horseradish
      peroxidase • tracer • astrocyte • basal lamina

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