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Neu 257; Winter 2010In Celebration of Darwin
Natural Selection and Conservation of Brain Circuits:
Alternate Migration and the Origins of the Mammalian Neocortex
Harvey J. Karten
University of California San Diego
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Evolution of Sensory Projections Upon “Cortex”
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Sensory Representations on Cortex
• Olfactory
• Visual
• Auditory
• Somatosensory
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Theories of Telencephalic Organization Prior to 1960’s
• 1) Telencephalon as a derivative of the Olfactory System – Archi/Paleo Cortex
• 2) Birds/Reptiles: Mostly striatum• 3) “Neocortex” as a uniquely mammalian
expansion• 4) The brain rewires in the course of evolution
(Out with the Old and In with the New)
• WRONG, WRONG, WRONG & WRONG!
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Yet Another Myth
• When you find “profound” similarities in brain nuclei, circuits and behaviors in different classes of vertebrates, it shows the wonder of Convergence/Parallelism!
• This logic does not pertain to the genome, and if the genome controls the wiring of the brain, why should be so quick to adopt a Crypto-Theological view of brain evolution?
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Did “Neocortex” Arise As A Novel Product of Mammalian Evolution?
• Where did all those specific neurons of brainstem, thalamus and cortex come from?
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Darwin (1809-1882)
The Origin of Species (24 November, 1859)
“I have called this principle, by whicheach slight variation, if useful, is preserved,
by the term Natural Selection.”
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Visual Cortex
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Rat Brain
Basal Ganglia
Cortex
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Pigeon Brain: Lateral View
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Studying Evolution of the Nervous System
• 1) What has evolved? Are there any evident precursors?
• 2) What are the molecular determinants of change?
• 3) What are the physiological and behavioral manifestation of those changes?
• 4) What are the driving forces of the change?
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Proposition: Cortex did not evolve de novo with the appearance of
mammals.
•Cortical evolution can be analyzed as three related problems:
–1) The history of the constituent neurons and connections of the cortex–2) The laminar apposition of these populations. –3) Microcircuitry underlying information processing
•What are the molecular mechanisms of each of these events?
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Rat Brain
Basal Ganglia
Cortex
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Where is the "real" striatum?
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Evolution of the Mammalian Sensory Systems &Cortical
Pathways• How does the mammalian auditory & visual system evolve?
•This can only be addressed by first understanding what may be the ancient pattern of organization of e.g., the vertebrate auditory & visual systems, and then identifying those cell and circuit properties that may be unique and novel amongst mammals.
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The Nature of Mammalian Neocortex
•Peripheral sensory inputs reach the thalamus, and thalamus projects upon the cortex
•=========
•A simple model:
•Thalamic recipient neurons (e.g., Layer IV)
•Interneurons (e.g., Layers II-III)
•Cortical Descending Efferents (e.g., Layers V-VI)
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Transposition/Migration during Development
Karten 1969, 1970
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Karten 1969, Nauta & Karten 1970
Transposition/Migration during Development
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Molecular Markers & the DVR Hypothesis
Recent studies of molecular markers reveal extensive similarities between cells of the DVR and those of individual layers of the mammalian ‘neocortex’ (Dugas Ford and Ragsdale)
In addition to EAG, RORbeta, Type III Tubulin, the DVR and the Cortex both express Ngn 1 and 2 as well as many other regulatory genes.
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Layer 4 Markers:
Eag2/Kcnh5
Layer 4 Marker: RORbeta
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Field LLayer 4 Markers:
Eag2/Kcnh5
Layer 4 Marker: RORbeta
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Computational Implications
•What are the advantages, if any, of lamination?
•What unique properties does lamination confer upon those animals?
•Have we overstated the virtues of laminar structures?
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Properties of Cortex
•Laminar populations
•Specific Afferentation and Efferentation
•Differential morphology and molecular properties
•Radial/columnar organization
•Recurrent loops
•Re-entrants
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The Radial Hypothesis: Columns
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The Radial Hypothesis Revisited I.
•The concept of columns and modules proved of great heuristic value in physiolgical investigation of the mammalian cortex. (Lorente de No, Mountcastle, Hubel & Wiesel)•Rakic postulated a radial unit hypothesis to explain the development of columns and modules•However, the evolutionary origins of the column and module in the forebrain were unknown.
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Radial and Columnar Organization in the Avian DVR
• Auditory pathways to the telencephalon:– Nucleus ovoidalis thalami (Karten 1967)– Field L (Karten 1968) – Field L as homologue
of Layer IV of auditory cortex
• Tonotopic representation in Ovoidalis & Field L (Konishi and Zaretsky)
• Laminar subdivisions of Field L (L1, L2, L3, HV) (Bonke and Scheich, 1979)
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Tonotopic & Columnar Organization of Field L
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Evolutionary Origins of Radial Units
•Studies of the Auditory region of Field L with 2-DG, showed columnar monotonic organization (Bonke & Scheich 1979)
•Does columnar/radial organization exist in the Avian/reptilian DVR?
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Granular cells in L2aOther cell types
in L2a
20 micrometer
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Mammalian AI
I
II
III
IV
V
VI
Non-auditory inputsICc ICx
MGvNon-auditory inputs
MGmPINMGd
Lemniscal pathway
Nonlemniscal pathway
Amygdale
Auditory inputAuditory input Non-auditory inputsMLd ICo
OvNon-auditory inputs
Avian auditory cortex
L2
Nd & Ai
L3
HV
L1
Lemniscal pathway
Nonlemniscal pathway
“Ov Shell”
Descending projections Descending projections
FunctionalModular
FunctionalModular
Amygdale
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Evolutionary Origins of Radial Units
•Contrary to our long held beliefs, radial and columnar units exist in the DVR of nonmammalian vertebrates.
•These discoveries imply that graded degrees of lamination and radial-columnar interactions arose at an early stage of telencephalic evolution.
•Homologous computational components of cortical-equivalent neurons is most likely a property common to all amniotes. •HJK – May 2005
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What’s Next?
•What are the molecular events that determine these highly conserved properties of cells and circuits? What are the molecular events that mediate the modifications in alignment of these cells that lead to the evolution and development of the mammalian type of cortex?
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What is the significance for computational modeling of cortical processing?
• We still do not have an accurate map of the circuitry of the cortex
• What is the implication for first order processing?
• What is the ratio of stellates to granule cells? (1:10 or greater?)
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Evolution, Connectomics & Natural Selection
Circuitry responsible for specialized functions is highly conserved.
Once established and operational, only minor changes generally appear.
The more detailed the similarities, the greater the likelihood of common origin
Natural Selection narrows the prospects for major changes in circuitry and function
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Connectomics and Genomics
How are connections, transmitter/receptors, cell morphology, ion channels specified during embryogenesis?
How are the vast numbers of specific neurons and connections encoded in the genome
To what extent are they subject to environmental modification and/or differences between individuals of a species?
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Stability, Species Changes, Individuality, and Evolution of
Circuits• Neural circuits underlie all operations of the brain• Neural circuits are both highly conserved, but also the
target of vast expansion (and loss) in the course of evolution and individual aging.
• Specific circuits are often unique to individual species
• Many circuits are common to virtually all vertebrates
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Genomics, Connectomics and Evolution
• The paradox of neural circuitry – conservation and change.
• Enormous variation within a highly conserved core set of properties
• The conserved properties imply genetic regulation• How is this encoded in the genome?• “Inherited musical or mathematical abilities” – is
this “in the genes” that regulate neural circuitry
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A Few Postulates About Evolution and Circuitry
• Primary Sensory and Motor Processing is highly conserved (initial stages of cognitive processing)
• Homologous circuits operate in similar manner• Homologous circuits mediate similar “core” behaviors• Closely similar behaviors have high probability that they are
mediated by homologous circuits• This is true for central visual, auditory, somatosensory
pathways from periphery to telencephalon.• Equally true for descending projections from telencephalon• At this time, we have few ideas about how neural cell
typology and connections are encoded in the genome.
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Connectomics and Genomics
• How are connections, transmitter/receptors, cell morphology, ion channels specified during embryogenesis?
• To what extent are they subject to environmental modification
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Henry Beston’s Outermost House
“We need another and a wiser and perhaps a more mystical concept of animals. Remote from universal nature, and living
by complicated artifice, man in civilization surveys the creature through the glass of his knowledge and sees thereby a feature magnified and the whole image in distortion. We
patronize them for their incompleteness, for their tragic fate of having taken form so far below ourselves. And therein we err, and greatly err. For the animal shall not be measured by
man. In a world older and more complete than ours they move finished and complete, gifted with extensions of the senses we have lost or never attained, living by voices we
shall never hear. They are not brethren, they are not underlings; they are other nations, caught with ourselves in
the net of life and time, fellow prisoners of the splendour and travail of the earth.”
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Nothing in Biology Makes Sense Except in the Light of Evolution
Theodosius Dobzhansky, 1973
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William Hodos
Walle Nauta
Anton Reiner
Nicholas Brecha
Yuan Wang
J. Martin Wild
Agnieszka Prechtl
Jorge Mpodozis
Harald Luksch
Jaap Dubbeldam
Locations:
WRAIR
MIT
SUNY
UCSD