Hello. I’m Michael Farries, a graduate student of David Perkel. I have been,
until now, a silent member of the Avieaters/Bird Nomenclature group. I’ve decided it’s
time for me to speak up. It’s evident that while homologizing mammalian and avian
pallium is extremely contentious, there has been general agreement that the basal ganglia
(BG) can be more easily compared, and thus a homology-based system of nomenclature
for the avian BG is within reach. Since there has been disagreement about virtually every
other aspect of the nomenclature, it’s important that someone disagree about this, if only
to maintain symmetry. I’ve decided to step up to the plate. Before I proceed, I would
like to remind my gentle readers that issues I raise here were largely acknowledged in the
Striedter/Perkel proposal. I, however, come to somewhat different conclusions on how
this should affect nomenclature proposals.
The excellent anatomical and histochemical studies of the avian BG over the last
30 years, starting with Harvey Karten and continuing with the work of Anton Reiner,
Loreta Medina and other colleagues has revealed an avian subpallium that is surprisingly
similar that of mammals. The bulk of the avian subpallium can be divided into a striatum
(PA, LPO) and pallidum (PP) that are hodologically and histochemically very like their
mammalian counterparts (striatum: caudate, putamen, nucleus accumbens; pallidum:
globus pallidus/GPe, entopeduclular nucleus/GPi, ventral pallidum). There are some
differences, of course, as one must expect for lineages that have been separate for 300
million years. For example, the avian pallidum (PP) doesn’t seem to be divided into
internal and external segments as it is in mammals (Reiner et al., 1998), and PA (or least
caudalmost PA) lacks ChAT+ neurons (Medina and Reiner, 1994 and personal
observations).
There’s another key difference between at least parts of the avian striatum and
mammalian striatum. Mammalian striatum generally communicates with the thalamus
via the pallidum, but does not project to the thalamus directly. In contrast, a specialized
part of oscine LPO associated with the song system (area X) projects directly to the
thalamus, as does a part of psitticine LPO (LPOm). To a mammalian BG aficionado, this
is a big deal. Some people even take this as a demonstration that these structures could
not be striatal. One might be tempted to write this off as an odd specialization of the
song system, but the fact that a striatothalamic projection appears in two systems (the
vocal control systems of songbirds and parrots) that seem likely to have evolved
separately (Striedter, 1994; Farries, 2001) argues against this. Furthermore, I’ve recorded
“pallidum-like” neurons that morphologically resemble the thalamus-projecting neurons
of area X both within area X and far outside of it, scattered throughout zebra finch PA
and LPO (Farries and Perkel, 2000 and 2002). Finally, I’ve observed retrogradely
labeled neurons throughout zebra finch LPO following thalamic tracer injections in the
vicinity of DLM (I have a poster on this at Neuroscience this year), and these neurons
also morphologically resemble the pallidum-like neurons I’ve recorded in brain slices.
Thus, a substantial part of the avian striatum outside of specialized vocal regions
seems to constitute a striatum/pallidum hybrid, unlike the mammalian dorsal striatum as
it is currently understood. It’s not clear how widespread this phenomenon is in Aves, but
it’s certainly not limited to passerines given the known anatomy in parrots. Now the
question is, what impact does this have on inferring homology in the avian BG, and how
might this affect nomenclature proposals? It is still possible that this is simply a derived
characteristic of avian dorsal striatum, and thus would not greatly disturb its proposed
homology with mammalian dorsal striatum. But I think there are other possibilities. To
motivate this, consider the status of the avian pallium. Whether you subscribe to
Karten’s hypothesis or Puelles’s or something else entirely, you have to invoke
substantial reorganization during the evolution of the amniote telencephalon to explain
the relationship between the mammalian and avian pallium. Couldn’t this have involved
the subpallium too? Both Karten’s and Puelles’s points of view suggest alternatives to
the hypothesis that most of PA and LPO are homologous to mammalian dorsal striatum.
First, a hypothesis inspired by Karten’s cellular homology ideas. The last
common ancestor of mammals and birds might have had a distinct striatum and pallidum,
but at some point in the lineage leading to birds, some pallidal neurons began migrating
into the striatum. The pallidum-like, thalamus-projecting neurons of PA and LPO would
then be “cellularly homologous” to the mammalian pallidum. That in turn makes the
designation of PA and LPO as “lateral striatum” and “medial striatum” at least somewhat
problematic. Of course, it is possible that this pallidal migration phenomenon originated
after the emergence of Aves and is thus found in only a subset of avian taxa.
Now for a hypothesis related to Puelles’s viewpoint (I know it’s not fair to label
these points of view simply Kartenesque or Puellesocentric, but for the sake of brevity...).
As you know, this view has the telencephalon develop through patterning mechanisms
that are conserved throughout amniotes, but with different developmentally defined
compartments contributing to much of the pallium in adult mammals and birds
(mammals: dorsal pallium; birds: ventral and lateral pallia). Something similar might
happen in the patterning of the subpallium (molecular mechanisms as yet undefined),
perhaps related to the shift in patterning in the pallium, perhaps independent of that. To
clarify: the amniote subpallium might be divided into different developmentally defined
compartments, with different compartments contributing to the bulk of the subpallium in
adult mammals and birds.
What are these “compartments”? The striatum and pallidum seem to arise from
different compartments defined by the presence (pallidum) or absence (striatum) of
Nkx2.1 expression, but I am suggesting that there are other subpallial compartments
whose “patterning molecules” are currently unknown. Outside of the striatum and
pallidum, the subpallium consists of the septum (or at least part of it) and bewildering
mix of basal forebrain structures including the central and medial nuclei of the amygdala,
the sublenticular substantia innominata, bed nucleus (or “nuclei”) of the stria terminalis,
etc. As far as I know, there are two schools of thought on how these basal forebrain
structures fit into the subpallial scheme. One, led by Larry Swanson, holds that the entire
subpallium can be divided into striatal and pallidal parts, so each of these basal forebrain
structures or their subdivisions can be classified as one or the other (Swanson believes
this applies to the septum as well, where the lateral septum is striatal and the medial
septum pallidal). The second school of thought, championed by Lennart Heimer, George
Alheid, José de Olmos, et al., consider most or all of these structures as parts of a larger
entity called the “extended amygdala.” As far as I can tell, they regard the extended
amygdala as distinct from both striatum and pallidum, so that the subpallium comes in at
least 3 separate flavors (I’m not sure what they would say about the septum). The
interesting thing about the “extended amygdala” for the purposes of this discussion is that
while many of these structures resemble the striatum in certain ways, they also have
“nonstriatal” projections to the brainstem and diencephalon (usually hypothalamus, not
thalamus). My second alternative hypothesis on avian BG homology holds that much of
PA and LPO are homologous to “extended amygdala,” not striatum.
Time to backpedal. There are lots of obstacles to this hypothesis, many related to
hodology. These extended amygdala structures have projections related to their visceral
and limbic functions, while at least large chunks of PA and LPO are more sensorimotor.
Second, there are lots of similarities between mammalian dorsal striatum/pallidum and
avian PA-LPO/PP that make the case for their homology pretty compelling. I can
partially address objection number one by saying that almost any theory of telencephalic
evolution in amniote lineages is going to have to invoke a lot of anatomical divergence,
and this hypothesis is no exception. Just think of the task relating the mammalian
claustrum, piriform cortex, and pallial amygdala to avian archistriatum, neostriatum, and
hyperstriatum ventrale. The second objection is more difficult to address in a reasonable
amount of space, but I think that a version of my “second hypothesis” could be
formulated that is at least as parsimonious as the PA-LPO = dorsal striatum hypothesis.
I’m not saying that I think my “second hypothesis” is true in the form I’ve presented it;
I’m not even saying that I think the dorsal BG homology hypothesis is false. I am saying
that reasonable alternative hypotheses on BG homology are possible given the current
data. It may not be a great idea to base a new nomenclature on a homology hypothesis
that is open to reasonable doubt. I’m not unalterably opposed to calling PA “lateral
striatum,” LPO “medial striatum,” and PP “pallidum,” but that scheme does have a
downside that should be recognized. The least of the various evils might be simply to
stick with the current (subpallial) nomenclature... that, at least, maintains continuity with
the past literature. Unless you prefer “hyperextended striatoamygdalum.”
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Brain: Lessons Learned from Comparative Neurobiology. Brain Behav Evol
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Farries MA, Perkel DJ (2002) A Telencephalic Nucleus Essential for Song Learning
Contains Neurons with Physiological Characteristics of Both Striatum and Globus
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