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The Journal of Neuroscience, February 1, 2002, 22(3):612-613
MINI REVIEW
Neurogenesis in the Adult Brain
Fred H.
Gage
Laboratory of Genetics, The Salk Institute, La Jolla, California
92037
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ARTICLE |
A milestone is marked in our
understanding of the brain with the recent acceptance, contrary to
early dogma, that the adult nervous system can generate new neurons.
One could wonder how this dogma originally came about, particularly
because all organisms have some cells that continue to divide, adding
to the size of the organism and repairing damage. All mammals
have replicating cells in many organs and in some cases, notably the
blood, skin, and gut, stem cells have been shown to exist throughout
life, contributing to rapid cell replacement. Furthermore, insects, fish, and amphibia can replicate neural cells throughout life. An
exception to this rule of self-repair and continued growth was thought
to be the mammalian brain and spinal cord. In fact, because we knew
that microglia, astrocytes, and oligodendrocytes all normally divide in
the adult and respond to injury by dividing, it was only neurons that
were considered to be refractory to replication. Now we know that this
long accepted limitation is not completely true, because there are two
rather discrete areas of the brain, the dentate gyrus of the
hippocampal formation and the subventricular zone and its projection
through the rostral migratory stream to the olfactory bulb, which can
generate new neurons.
Although the discovery that there are limited areas of the brain where
neurons do regenerate is important, it also deepens our curiosity as to
why it is that most neurons in fact cannot replicate. One reason why
neuronal replication in the adult was considered unlikely was the
complexity of most neurons; with their highly branched dendrites and
polysynaptic axonal combinations, they were considered to be terminally
differentiated and unable to re-enter the cell cycle and divide,
strictly from a mechanistic view. Another problem was conceptual. If
neurons were able to divide, how would the newly created cells with
their new dendrites, axons, and synapses, functionally integrate into
the brain without disrupting existing circuits? With the dominant
theories of brain function being based on a computer analogy with fixed
circuits, it did not seem at all logical that adult brain circuitry
could be continually adding new components.
Several recent discoveries and refinements of our conception of the
brain have converged to help make the concept of neurogenesis in the
adult brain more easily acceptable.
The mechanical problem of accommodating the dividing neurons has been
overcome by the discovery that neural stem cells exist throughout life
in the adult brain and can renew and give rise to new neurons,
astrocytes, and oligodendrocytes, just as in the developing brain. This
was first shown from the subventricular zone (Reynolds and Weiss, 1992 ;
Richards et al., 1992) and then in the dentate gyrus of the hippocampus
(Gage et al., 1995; Palmer et al., 1997), and in most structures of the
brain examined (Palmer et al., 1995; Shihabuddin et al., 2000), even
where no neurons existed (Palmer et al., 1999; Kondo and Raff,
2000).
These studies demonstrating that cells with stem cell properties exist
in the adult brain were conducted in vitro, so it is not
clear whether these cultured cells have the same potential in
vivo as in vitro. Nevertheless, they showed that we no
longer had to consider that a complex neuron was required to divide for adult neurogenesis to occur. Now we know that these neurons can be
generated from primitive cells, similar to what happens in development.
A second change in thinking was more gradual and conceptual, and is
still not completely resolved. Almost as soon as the first computers
were made, the analogy with the brain was accepted. The model of the
brain as a computer, with hard-wired connections that are adaptive and
flexible mostly with respect to the software and with information that
is distributed over the hard-wired network still dominates.
The pervasive theory of adaptability or plasticity was provided by Hebb
(1949), who postulated that plasticity, and adaptability could be
accomplished by "strengthening synapses" without requiring structural reorganization.
A decade or so after the ascendance of the computer model of brain
circuitry, Altman (1962) made his original claim of neurogenesis, and a
theory of structural plasticity began to emerge. Soon afterward, examples of axonal elongation and synaptic reorganization in response to injury were provided (Raisman, 1969; Moore et al., 1971; Lynch et
al., 1973). Within the same time period, investigators demonstrated that experience alone could promote structural changes in presynaptic and postsynaptic elements (Greenough et al., 1978).
The willingness to accept adult neurogenesis was further enhanced by
the convincing evidence that fetal tissue could be grafted in the adult
intact brain. Even more convincing was the evidence that the damaged
adult brain and spinal cord allowed these newly grafted cells to
survive and differentiate (Bjorklund and Gage, 1985). The grafted cells
could also receive and send connections and release transmitter in a
behavior- dependent manner in the adult damaged brain (Dunnett and
Bjorklund, 1994)
The stage has been now set for accepting the ability of stem cells in
the adult neuronal system to give rise to neurons. In addition, the
damaged adult brain appears to retain enough potential to accept, if
not participate in, the differentiation of developing cells into
functional neurons.
The authors of the following mini-reviews are significant contributors
to the current re-emergence of adult neurogenesis. There are several
themes that the authors have independently identified. First, they each
have presented a historical perspective that helps explain how their
view of this field developed. Although it is likely that a field as
young as this is searching for it origins, it is likely that it will
take more time for the field to reveal its historically relevant origins.
A second theme that emerges from these reviews is the concern over the
techniques that are used to document the neurogenic events that are
being reviewed and examined. Each of these authors has contributed to
the continued development of the tools, but it is clear that more and
better methods are needed to quantitatively document the birth,
proliferation, and migration of the new neurons and provide evidence
for the extent to which new neurons functionally integrate into the
adult brain. Will better techniques reveal more neurogenesis in more areas?
Another theme that all of the authors developed and acknowledge is the
remarkable extent to which the environment in which the adult animal
finds itself, and in particular how the organism behaves in that
environment, can affect the birth rate and fate of the newly born
cells. Is it possible that, with the appropriate behavioral and
environmental stimulation and more accurate techniques, neurogenesis
will be revealed or induced in other regions previously considered
non-neurogenic? Or will they give insight into the mechanisms that
limit neurogenesis in different brain regions, and by so doing, lead to
ways to circumvent those mechanisms?
A series of questions related to the identity of the endogenous cells
as they transition from the most primitive stem-like cell to the most
mature neuron is currently being very intensely investigated and
debated. The answers to those questions may surprise us and force a
re-evaluation of our current understanding of stem cell or precursor
biology. Clearly there are lessons to be learned from developmental
biology, in which the process and mechanisms of neurogenesis have been
the topic of intense investigation for decades. A fundamental question
raised in the last review asks to what extent the mechanisms of
neurogenesis in development and in the adult are the same. Given the
wealth of knowledge available in developmental biology, this should be
a tractable problem.
Finally, the two unresolved questions that all agree on are: (1) why
does adult neurogenesis persist in only a few identified brain regions
and, even more perplexing, (2) what is the function that underlies this
residual structural plasticity?
Solutions to the first question will likely require a comparative
approach, which considers the evolutionary development of these
structures. The second question of function will likely require a
reconceptualization of neural plasticity that incorporates structural
plasticity into its theoretical framework. A more complete answer to
either of the questions will require a better understanding of the
normal function of the hippocampal formation and olfactory bulb and
their local circuits. Perhaps a better understanding of the process of
neurogenesis within these structures will elucidate more completely the
functions these more global structures subserve.
The series begins with Pasko Rakic and Elizabeth Gould discussing the
strengths and limitations of the methodologies used to identify cells
undergoing neurogenesis in the mammalian dentate gyrus of the
hippocampus. Fernando Nottebohm describes the perspective from work on
avian brains, which have shown prominent abilities for neurogenesis in
the adult. Arturo Alvarez-Buylla discusses a system in the mammalian
brain, the anterior migratory stream, that continues to generate new
neurons during adult olfactory bulb, and he discusses recent work on
the origin and phenotype of the initiating cell. Gerd Kempermann
returns to neurogenesis in the dentate gyrus and focuses on the role of
behavioral activity on the regulation of adult neurogenesis, and
he discusses the functional significance of this process in the
hippocampus. Finally, Chris Kintner summarizes the key elements and
principles of neurogenesis that have been revealed from the extensive
developmental neurobiology literature, and he makes parallels
with adult neurogenesis. Importantly, this last review leads to some
specific hypothesis and prediction when determining whether adult and
developmental neurogenesis are equivalent.
| |
FOOTNOTES |
Correspondence should be addressed to Dr. Gage at the above address.
E-mail: gage{at}salk.edu.
| |
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Copyright © 2002 Society for Neuroscience 0270-6474/02/223612-02$05.00/0
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