I’m teaching a course in neurobiology this term, and it’s strange how it warps my brain; suddenly I find myself reaching more and more for papers on the nervous system in my reading. It’s not about just keeping up with the subjects I have to present in lectures (although there is that, too), but also with unconsciously gravitating toward the subject in my casual reading, too.
“Unconsciously”…which brings up the question of exactly what consciousness is. One of the papers I put on the pile on my desk was on exactly that subject: Evolution of the neural basis of consciousness: a bird-mammal comparison. I finally got to sit down and read it carefully this afternoon, and although it is an interesting paper and well worth the time, it doesn’t come anywhere near answering the question implied in the title. It is a useful general review of neuroanatomical theories of consciousness—even if it left me feeling they are all full of crap—but in particular it’s an interesting comparative look at avian brain organization.
The paper briefly reviews four classes of models that attempt to locate the centers of consciousness, or “consciousness generators”, in the mammalian brain. Alas, they all seem to contradict one another, and are all driven by the authors’ hypotheses to invent validation in the structure, rather than by actual data that might lead to useful hypotheses. I won’t get into these, other than to paste in the summary—while I’m not at all dazzled by any of them, it is handy to have such tidy summaries.
Classification of consciousness—brain
Bottom-up Top-down Sensory systems A B Motor systems C D
A: A representative bottom-up theory proposed by Crick
and Koch concerns the visual system and asserts
that visual awareness is associated with activity in higher
order visual areas that are in direct contact with prefrontal
cortex. Although the “cortical system” covered by this
theory includes the entire cerebral cortex, dorsal thalamus,
claustrum (a nonlaminated structure deep to the cortex),
and dorsal striatopallidal complex (caudate, putamen,
globus pallidus—also referred to as basal ganglia and
involved in motor control) in the forebrain as well as
the motor control-related cerebellum and various brainstem
projection systems, the generator neurons seem to be
limited to temporal, parietal and prefrontal regions of the
neocortex. Crick and Koch limit the generator structure
further by assuming that activity in a subpopulation of
neurons in cortical layer V, characterized by firing in burst
patterns, is crucial. A prominent feature in the theory of
Crick and Koch is the insistence that the primary visual
cortex is not a generator structure.
B: The theory of Edelman and Tononi appears to
be an example of a top-down sensory approach and
focuses on the general features of consciousness—such
as complexity and unity. It asser ts that consciousness is
associated with activity in the temporal and frontal
associative and motor regions of the cortex: a “dynamic
core”, characterized by “re-entrant” interactions within
limited portions of the CNS. Possibly, thalamic neurons are
included in the dynamic core. Structures supporting the
dynamic core seem to be the septal region, amygdala,
hippocampus, dorsal thalamus, and hypothalamus within
the forebrain, as well as the reticular activating
system in the brainstem. Edelman and Tononi seem to
assume a larger and more dynamic population of generator
neurons than Crick and Koch. In comparison to the latter,
the inclusion of limbic system structures—septal region,
amygdala, and hippocampus—that are related to emotion
and learning make this theory more broadly based.
C: The theory suggested by Eccles may be said to
represent a bottom-up approach, largely based on studies
of the motor system. It takes consciousness to be
associated with activity in cortical columns of the pre- or
supplementary motor areas, for med by groups of generator
pyramidal cells, organized in a specific way (dendrons).
This means that Eccles’s theory assumes the smallest and
most well defined population of generator neurons of all the
theories discussed here.
D: The theory formulated by Cotterill may be said to
be an example of a motor system top-down approach.
According to this, consciousness is associated with
activity in a circuit consisting of sensory and motor, cortical
and thalamic structures. Fast feedback from muscle
activity, making muscle spindles (sensory receptors for
the degree of stretch within muscles) critical for the
generation of consciousness, is a central par t of the
theory. Fundamental to Cotterill’s, as well as to other
top-down theories, is a set of proposals implying that the
neural basis for consciousness lies in the ability of an
organism to know itself, or its proto-self, within its environment, by bodily movements and homeostatic
functions. In all these top-down theories, several
non-cortical regions seem to be included in the generator
structure of consciousness. Cotterill includes the amygdala, hippocampus, dorsal thalamus, subthalamus, hypothalamus, and dorsal striato-pallidal complex (caudate,
putamen, and globus pallidus) within the forebrain
as well as multiple brainstem structures—the superior
colliculus (involved in sensory and motor mapping of
space), various structures involved with motor system
regulation (cerebellum, substantia nigra, pontine nucleus,
red nucleus, and inferior olive), and part of the autonomic
nervous system (for control of visceral functions)—thus
for ming a larger generator structure than any other theory
discussed here. Additional motor system top-down ap-
proaches include that of John, who includes the
thalamus, limbic system, and dorsal striato-pallidal complex, and that of Parvezi and Damasio,(24) who incorporate
the hypothalamus, intralaminar and reticular nuclei of the
dorsal thalamus, basal forebrain, and various cholinergic,
glutamatergic, noradrenergic, dopaminergic and serotonergic projection systems that regulate the activity of the
There’s also a diagram of where these theories place the “conciousness generators” (in dark gray) in the human brain. As you can see, they all agree it is not in the brainstem or cerebellum, but from there anything goes.
The more productive part of the paper is the comparison between mammals and birds. Here’s the premise:
that, since highly complex cognitive abilities are correlated with
presumed consciousness in at least some mammals, including but not limited to humans, and since highly complex cognitive abilities are evinced by birds, it is likely that consciousness
is also present in birds. Given that hypothesis, we then can
compare the anatomical organization of mammalian and avian
brains. We reason that if (1) complex cognition and consciousness are present in both mammals and birds and (2) consciousness has any neural basis, then birds should have at
least some neural features in common with mammals to
That sounds promising, but several problems come to mind. 1) If no one can even agree on the neural features responsible for consciousness within mammals, how is this comparison going to identify commonalities? 2) Birds and mammals are related lineages, so many brain similarities are going to be consequences of shared history, not function. Why not go all out and compare more distinct lineages…say cats and octopus? 3) Since we don’t even know what features of the areas of the brain are responsible for consciousness, we aren’t going to be able to recognize if different regions in birds and mammals have independently acquired whatever mysterious property is involved. While I think the comparative approach is terrific, in this case it’s premature and targeted at the wrong level.
But hey, you’ve got to start somewhere, and this wasn’t one of those exasperating papers that I toss into the wastebasket. It has a good summary of the evidence for avian intelligence, listing the various features they’ve exhibited.
- Transitive inference. You can train pigeons (Pigeons! Birds that are archetypically stupid!) to recognize rank order, such as that A<>B, and B<C, and they can use that information to recognize tha A<C.
- Coherence. Pigeons can respond variably to the ambiguity in figures like the Necker cube. That suggests that they have a mental model of what it should be, and their impression of its orientation can “flip”.
- Episodic memory. Scrub jays can recollect when, where, and what is stored in their food caches.
- Piagetian object constancy. Doves, magpies, parrots, and ravens aren’t fooled if an object is hidden—despite being out of sight, they have a mental model of its position.
- Cognitive abilities. Gray parrots are singled out as particularly brilliant, with individuals able to count to 7, recognize the concept of “none”, and able to understand the concepts of “same” and “different”.
- Tool use. Ravens, parrots, and New Caledonian crows have all been shown to be able to make and use simple tools.
- Theory of mind. Scrub jays are able to attribute their own predilections to other members of the same species. Jays that rob caches are more likely to move their own caches than “honest” jays.
While I have my doubts about the neuroanatomical comparisons, the authors bring up one very general point. In mammals, the neocortex—the hugely enlarged part of our forebrains that is the first thing you see when you crack open our skulls—is central to higher level thinking. The comparable structure in birds is called the hyperpallium, or Wulst (German for “bulge”), and the posterolateral portion of it is an important visual center, comparable to the striate cortex, or visual areas of our brain. The fascinating thing is that the cellular organization of these two areas with similar functions and perhaps similar roles in generating consciousness are very different.
The mammalian visual cortex is characterized by a beautifully layered organization. Different inputs segregate to different layers, and pyramidal neurons extend long dendrites orthogonal to those layers, like long antennae reaching up and sampling incoming data streams, each of which is segregated spatially. The Wulst, on the other hand, is organized like other nuclei of the brain, and the primary neurons are star-shaped, reaching out in all directions to contact their inputs. They lack the rigid but elegantly arrayed spatial segregation seen in us mammals.
The pictures below don’t really do it justice, but a good neurohistologist (sometimes even a barely adequate one, like me) can pick out 6 discrete layers in an appropriate slice of mammalian visual cortex. The bird Wulst is alien-looking. Huge, but weird.
In their conclusion, the authors are a bit vague about the relevance of the earlier theories of consciousness to bird neuroanatomy. Parts fit, others don’t, but since I think the theories are so nebulous that it’s nearly impossible to draw any conclusions from that, they can’t come down strongly one way or another. One suggestive observation is that bird brains are more similar to reptilian brains than mammalian brains are to stem amniotes’. If birds are conscious, that makes the assumption that the capacity for consciousness arose at that stem amniote-mammalian border suspect. The capacity, in the sense of having neural circuitry that could be adapted to generate consciousness, could have been present earlier.
Ann B. Butler, Paul R. Manger, B.I.B. Lindahl, Peter Århem. Evolution of the neural basis of consciousness: a bird-mammal comparison (p 923-936).