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A critical review of past and current theories of mammalian brain evolution is presented in order to discuss conceptual problems that persist in the field. Problems with the concept of homology arise because of the interaction of cell lineages and axonal connectivity in the determination of structural features of the brain. Focusing on the continuity of information represented by ontogenetic mechanisms as opposed to morphological features avoids many of these problems and suggests homological relationships that otherwise have gone unnoticed. Many apparently progressive trends and parallelisms in mammalian brain evolution turn out to result from the influence of underlying developmental homologies. Confusions about evolutionary advancement, increasing architectonic differentiation, and the evolution of new brain structures result from a failure to appreciate how increasing brain size can bias developmental processes with respect to axonal competition, increased cellular metabolic demands and decreased information processing efficiency. Explanations of the evolution of novel structures and new connectional patterns are criticized for their failure to consider the constraints of neural developmental processes. The correlations between structural neogenesis, functional specialization and size changes in brain evolution are explained by a theory of competitive displacement of neural connections by others during development under the biasing influences of differential allometry, cell death or axon-target affinity changes. The “displacement hypothesis” is used to propose speculative accounts for the differential enlargement and multiplication of cortical areas, the origins of mammalian isocortex, the unusual features of dolphin cortex and the dramatic structural and functional reorganizations that characterize human brain evolution.
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Rethinking Mammalian Brain Evolution
1
Harvard University, Peabody Museum, Cambridge, Massachusetts
02138
S
YNOPSIS
.
A
critical review of past and current theories of mammalian brain evolution
is presented in order to discuss conceptual problems that persist in the field. Problems
with the concept of homology arise because of the interaction of cell lineages and axonal
connectivity in the determination of structural features of the brain. Focusing on the
continuity of information represented by ontogenetic mechanisms as opposed to mor
-
phological features avoids many of these problems and suggests homological relationships
that otherwise have gone unnoticed. Many apparently progressive trends and parallelisms
in mammalian brain evolution turn out to result from the influence of underlying devel
-
opmental homologies. Confusions about evolutionary advancement, increasing architec
-
tonic differentiation, and the evolution of new brain structures result from a failure to
appreciate how increasing brain size can bias developmental processes with respect to
axonal competition, increased cellular metabolic demands and decreased information
processing efficiency. Explanations of the evolution of novel structures and new connec
-
tional patterns are criticized for their failure to consider the constraints of neural devel
-
opmental processes. The correlations between structural neogenesis, functional special
-
ization and size changes in brain evolution are explained by a theory of competitive
displacement of neural connections by others during development under the biasing
influences of differential allometry, cell death or axon
-
target affinity changes. The
"
dis
-
placement hypothesis
"
is used to propose speculative accounts for the differential enlarge
-
ment and multiplication of cortical areas, the origins of mammalian isocortex, the unusual
features of dolphin cortex and the dramatic structural and functional reorganizations that
characterize human brain evolution.
I
N
T
R
O
D
U
C
T
I
O
N
Intrinsic difficulties
Despite the fact that the evolution of the
brain
-
particularly the human brain
-
is
of intrinsic interest to anyone curious about
the human mind and the origins of human
nature, the scientific study of brain evo
-
lution is not a major subdiscipline within
biology, psychology, anthropology or even
the neurosciences. The apparently poor
representation of this area of study in the
sciences can in part be attributed to the
paucity of direct paleontological evidence
regarding brain evolution and the long
-
time inaccessibility of crucial comparative
neuroanatomic details. The poor repre
-
sentation of information about brain evo
-
lution in disciplines outside the neurosci
-
ences is additionally limited by the
considerable sophistication in comparative
neuroanatomy and physiology that is
required to even begin to grapple with the
questions in a meaningful way. The dis
-
turbing correlate of this is that speculative
theories concerning brain evolutionó
especially human brain evolution
-
are
widespread and often contain relatively lit
-
tle neuroanatomical or neurophysiological
information. But even theories conceived
by neuroanatomists and neurophysiolo-
gists often reflect numerous unsupported
assumptions about the direction of evolu
-
tionary trends, the nature of natural selec
-
tion affecting brain processes, the ways that
brains can vary from one species to another,
the relationship between structure and
function within the brain and even the
nature of intelligence itself. Although
paleoneurology is unlikely to experience
sudden advances in the years to come, many
of the barriers to relevant neuroanatomi-
cal evidence have dissolved in the wake of
the introduction of many new experimen
-
tal techniques in recent decades. Now that
many of the technical impediments stand
-
'
From the Symposium on
Science as a Way of Know
-
i
n
g
in
the
way
of
detailed knowledge about
ing
-
Neurobiology and Behavior
organized by Edward
S.
Hodgson and presented at the Centennial Meeting
brain structure and function have been
of the American Society of Zoologists, 27
-
30 Decem
-
removed, many of these hitherto unques-
ber
1989,
at Boston, Massachusetts.
tioned assumptions are now open to test.
Among colleagues in the neurosciences
one sometimes hears the criticism that,
unlike most other areas of neuroscience,
the study of brain evolution is limited to
theory because it is essentially beyond the
reach of experimental approaches.
Although brains of extinct species are not
available for direct inspection and analysis,
this does not necessarily mean that theories
of brain evolution are empirically untest-
able. Indeed they are every bit as suscep
-
tible to experimental investigation and
testing as are other theories of brain orga
-
nization and function. The approach must
necessarily be indirect, but it need be no
less effectual nor any less scientific or
experimental. We should remember that
the vast majority of scientific data in any
field is indirect, irrespective of whether the
object under study is directly observable.
From tracks left by subatomic particles in
nuclear accelerators to the measurements
of minute amounts of unseen biochemicals
registered in scintillation counters, nearly
all of the
"
hard data
"
generated in the
laboratories of any field of the natural sci
-
ences are indirect and circumstantial. It is
not the directness or indirectness of the
data that is important, rather it is the
repeatability of the findings and the coher
-
ence of many lines of evidence that are
crucial to scientific knowledge.
A good analogy to the study of brain
evolution is provided by the study of gene
evolution. Modern techniques for analyz
-
ing and comparing base sequences of DNA
molecules from living organisms are begin
-
ning to provide a truly astronomical fund
of information concerning both molecular
and organismal evolution. Without analyz
-
ing a single fossil specimen of DNA we are
nonetheless capable of reconstructing large
fractions of the genomes of extinct species,
characterizing major gene duplication and
reorganization events of the distant past,
and predicting the ancestral lineages of liv
-
ing species and the approximate dates of
their divergences. Al this is available today
despite the fact that only miniscule por
-
tions of the DNA in even the best studied
species are actually known and virtually
nothing is directly known about the DNA
of most species. This level of analysis is
made possible by the immensity and com
-
plexity of the existing genomes. In many
cases even direct fossil evidence of appar
-
ent phylogenetic relationships has been
abandoned in the face of contrary molec
-
ular information. As nearly limitless sources
of correlative molecular evidence are fed
into phylogenetic analyses in the near
future they will become immensely more
reliable for the determination of phylog
-
eny than the best of all possible fossil finds.
Living organisms are incredibly complex
systems at all levels of scale. Each molec
-
ular and organ system within an organism
embodies within its design the ubiquitous
mark of its particular evolutionary history.
In addition, the processes of embryogen-
esis that direct the construction of these
systems are themselves products and symp
-
toms of an evolutionary past that at various
levels intersects with the ancestries of other
species. Comparisons of the differences and
similarities among molecular systems,
organ systems and developmental pro
-
cesses in different species provide an almost
limitless source of information for inves-
tigating the evolution of biological struc-
tures. This is ultimately the final arbiter of
any analysis of evolutionary relation
-
ships
-
even for paleontological data—
since the interpretation of fossils is only as
accurate and complete as the information
we have about living counterparts.
The complexity of the vertebrate brain
rivals or exceeds the complexity of all the
other organ systems of the body consid
-
ered together. Because of this we should
expect that information derived from the
brains of living species will be more than
adequate to the task of investigating brain
evolution, so long as we are
willing and able
to approach the task with the level of
sophistication demanded by
it.
Given this
complexity and our still primitive under
-
standing of brain organizati'on and func
-
tion, we must be prepared to integrate
information from a variety of subfields of
neuroscience and evolutionary biology in
order to begin to approach the problems
of brain evolution with any clarity.
Although numerous researchers since the
nineteenth century have pursued the study
of brain evolution, most have focused on
a single source of evidence to support their
theories, including: relative brain size (e.g.,
apparent trends in brain size increase); fea
-
tures of cortical surface morphology (e.g.,
the appearance or reorganization of sulci);
relative sizes of macroscopic brain struc
-
tures with respect to one another (e.g., the
apparent enlargement of isocortex with
respect to limbic cortex in presumed
"
advanced
"
brains); or cyto
-
and myelo-
architectonic features (e.g., the apparent
enlargement of association cortex in the
cerebral cortices of
"
advanced
"
species).
But uni-dimensional approaches are almost
certain to lead into one misleading cul-de-
sac after another. This has been the fate
of many past theories, just as it will surely
also be the fate of the corresponding uni-
dimensional theories of the present. The
only hopeful approach is to integrate rel
-
evant information from many lines of neu-
robiological research that bear on the
questions of the patterns of variation and
constraint exhibited by the brains of dif
-
ferent species.
Experimental approaches
A number of recent technical advances
have significantly augmented the infor
-
mation previously available to comparative
neuroanatomists. Unlike many other organ
systems, the functionally relevant features
of brain anatomy are entirely microscopic
and for many decades were nearly impos
-
sible to distinguish even under the micro
-
scope. The axonal connections linking
neuron to neuron, though visible for short
distances in Golgi
-
stained material (avail
-
able since the turn of the century), have
only become amenable to study
in
recent
decades. In the 1950s techniques were per
-
fected for visualizing degenerating axons.
With these techniques it was possible to
identify the general patterns of long axonal
connections in the brains of experimental
animals. However, the resolution and sen
-
sitivity of these techniques were insuffi
-
cient to resolve many of the finer details
of axonal connection patterns. Beginning
in the mid 1970s a number of axonal trac
-
ing techniques were developed that took
advantage of the in vivo
uptake and axonal
transport. of amino acids, macromolecules
and certain fluorescent dyes. These tech
-
niques have now made it possible to inves
-
tigate the organization of axonal circuitry
in full microscopic detail. In this regard
the most basic functional anatomy of the
brain has at last become available for study.
We are still far from possessing a complete
connectional characterization for even the
best studied of mammalian brains, yet
already the scattered details from compar
-
ative studies have begun to provide a
remarkable array of new insights into the
patterns of brain diversity.
Now that tracer techniques have filled
this crucial gap in information about basic
neural functional anatomy, these data can
be integrated with data from physiological
and quantitative studies to provide all the
pieces of evidence necessary for investi
-
gating the principles underlying brain evo
-
lution. However, it is insufficient to apply
the analysis to adult brains only. Probably
the most crucial information for evolu
-
tionary purposes is how connection pat
-
terns and structural differentiation are ini
-
tially established in a developing brain. New
techniques for labeling mitotic cells, mark
-
ing cell lineages, and experimentally alter
-
ing development in neonatal animals or in
utero
by removing or transplanting embry
-
onic tissues are also beginning to provide
detailed information about the develop
-
mental processes that shape neural circuits.
Developmental information can play a cru
-
cial role in settling questions of homology.
More generally, it can provide evidence for
the range of possible mechanisms available
for natural selection to modify and dem
-
onstrates the constraints that limit possible
variation. Many scenarios of brain evolu
-
tion conceived in the absence of critical
information about the development of the
structures in question turn out to be incom
-
patible with these constraints.
This rapidly growing body of neuro-
biological information is providing an
unprecedented opportunity to discover new
patterns of similarity and variation in brain
evolution, and to test old and new hypoth-
eses about neural evolutionary