Comparative Neuroscience Research Paper

This question has frequently been investigated solely by comparing brain sizes. Specialists in comparative anatomy have also pointed out differences between major taxa, such as mammals and reptiles, in the layering of the cerebral cortex and the development of a corpus callosum, among other gross features. With the invention of a battery of new methods in experimental microanatomy that make possible the tracing of first order neuronal connections (those not interrupted by synapses), an extensive body of know-ledge has accumulated on comparative hodology—the projections into and out of identified brain regions, nuclei, and laminae. There is, in addition, a more limited literature on the comparison of neurally active compounds, such as transmitters and modulators, among the major taxa, including phyla.

Still less advanced is knowledge of mesoscopic and microscopic organization, including physiological as well as anatomical features that differ among animals, especially those relevant to behavior. Examples are: (a) cell types, especially those defined by response properties; (b) local circuits intrinsic to a nucleus or laminated structure; (c) the degree of reciprocity of connections between structures at the same level— such as cortico-cortical—and at different levels—such as thalamo–cortical; (d) dynamical interactions (potentiation, induced rhythms, event-related potentials, brain waves); (e) kinds of information processing (command cells, head-position compensating cells, pattern-sensitive cells, face-selective cells); and (f) emergent properties (kindling, seizures, learning of each of several kinds). Virtually unknown and awaiting future study are the neural substrates of behaviorally defined traits such as (g) the number and resolution of discriminable stimuli like individual voices, smells, and places within the environments experienced—roughly knowledge; (h) the number and qualia of emotions, sets, moods, and status symbols that an individual can manifest and can discriminate in others; and (i) the variety, specificity, and longevity of memories of past events.

This list, obviously, is not exhaustive and serves simply as a framework upon which to review the state of comparative neuroscience today.

1. Evolution Of The Nervous System

The nervous system and its sense organs and effectors have evolved through a greater span of complexity than any other system within living organisms, if we consider the animals with the simplest nerve nets and those with the most complex brains. It has not evolved linearly, steadily, or inevitably but with repeated instances of retrograde loss of complexity. But, overall and roughly, the more primitive taxa represented among surviving species have very simple nervous systems as well as behavior, relative to certain branches of the most derived taxa, which have extremely advanced (i.e., complex) brains and behavior.

This difference was already strong long before hominids or primates or mammals or vertebrates appeared. Even if we consider only gross anatomy and crude histology of the nervous tissue, a comparison of cnidarian medusae to polyclad flatworms, or of pulmonate snails to octopods, of agnathan hagfish to mormyrid teleosts, or of reptiles to mammals, dramatically underlines a diversity of grades of organization differing, above all, in complexity.

By complexity, in this context, we mean the sum of the kinds of elements and operations. This includes kinds of structural elements (distinguishable cell types on all possible criteria, plus groupings of cells, and structural parts with subdivisions at all levels), the kinds of functional connections and interactions, of physiological properties and influences, and of discriminable stimuli and behavioral actions. Each of these would be difficult to count but is concrete and not vague. On this tangible scale, one approachable by degrees, we can recognize higher and lower species, purely with respect to complexity.

We can thus estimate the degree of independence of evolution of traits and systems of traits, for example vision and movements, or vision and olfaction. We can approximate a distinction between major steps in grade (gastropods and cephalopods; reptiles and mammals), on the one hand, and on the other, adaptive specialization within roughly the same grade of overall complexity (e.g., life styles and adaptations among rodents or among bats). We can estimate that most evolution has been adaptation within grade, at the level of species, genera and families, whereas saltations in the major grades of complexity have been relatively few and clearest at the levels of (some) classes and (some) phyla. To see the big picture we should eschew arguable questions at the level of families and even higher taxa of roughly equivalent advancement, such as whether bats are a higher grade than rodents, or lobsters a higher grade than cock-roaches. It is best to compare phyla and classes, sometimes orders, choosing the most advanced species in each and avoiding taxa that might be secondarily simplified.

With these caveats, made to dispel charges of anthropocentric or moralistic, value-laden reasoning or a simplistic, linear animal scale, we can look at the grand sweep. Most of the time we scrutinize evolution with respect to how it happens, or how it is adaptive or what phylogenetic branching is most likely. We tend to overlook the perspective of consequences in terms of major grades of complexity. A grand fact of animal evolution is the development of more and more complex brains and, probably, also behavior—slowly and erratically, without a clear and self-evident in-crease in survival value but spanning an overall series of levels of advancement almost impossible to over-state.

The main thesis of this essay is that modern biology has neglected to study the details of the differences between grades of complexity. Beyond the gross and macroscopic anatomical differences in classical text-books, such as the mammalian hippocampus, corpus callosum, corticospinal tract, and six-layered viso-cortex, we lack an accumulated body of comparisons—at each of the relevant integrative levels from molecule to cognitive system. This is surely a rich vein of ore for future investigators to mine.

2. Macroanatomy and Connectivity

The state of knowledge of the gross and microscopic anatomy of the nervous systems of invertebrates (Bullock and Horridge 1965) and vertebrates (Butler and Hodos 1996, Nieuwenhuys et al. 1998) can be found in text and reference books, richly illustrated. Four levels of inquiry may be distinguished.

2.1 Brain Size

Brain size is the crudest, usually plotted against body size, since a regression of these two measures is general. Both measures have large uncertainties, including how much of the normal cerebrospinal fluid, blood, blood vessels and plexuses, meninges, and nerve roots should be included, how the brain was removed and pre-served, how body weight is taken and how exoskeleton, horn, shell, gastrointestinal contents, fat, preservative, and other variables are treated. The regression is characteristically very low for plots of individuals of the same species, substantially higher for species of the same family, and still higher for higher taxa. This makes compensating for size, sex, age, nutritive state, and cutaneous appendages only an approximation. The general result is clear—that brains considered more advanced on other criteria tend to be larger in proportion to the body. To an unknown extent the larger brains are considered to reflect greater sensory input and a larger variety of discriminable stimuli plus a greater efference and larger variety of responses. These, however, are essentially untested hypotheses and it can be seriously doubted that these factors adequately account for the size differences.

2.2 Brain Lobes And Nuclei

Brain lobes, clumps of nerve cells (nuclei), and gross subdivisions of these are potentially more meaningful than sheer size to compare across taxa, life style, and behavioral adaptations. Many examples are known where prominence of optic lobes, auditory nuclei, areas of the cortex representing snout or whiskers, bird-song centers, or hippocampal place-memory enlargements correlate with behavioral adaptations. Yet many other features of comparisons between species are not obviously explicable in terms of the known habits of life—as for extreme differences in cerebellar size among families of elasmobranchs, size diversity in the habenula and corpus striatum, or diversity of layering in visual cortex among primates and in the dorsal cochlear nucleus among rodents. This level of analysis might be expected to be more sensitive than others to behavioral complexity, especially in the degree of differentiation of the relevant brain parts. It seems likely that enumeration by equivalent standards of the number of distinguishable subdivisions of the thalamus or hypothalamus, or of the cortex as between reptiles and mammals—taxa at quite distinct grades of complexity—would show a greater variety in the mammals. But we have, so far, very few attempts to make such comparisons. This would quantify the strong impression from qualitative histology that the brains in the most advanced teleosts are more complex than those in the most advanced amphibians, as well as elasmobranchs.

2.3 Connections, Afferent And Efferent, Into And Out Of Each Nucleus Or Lamina

Connections, afferent and efferent, into and out of each nucleus or lamina, indeed each cell type, are now extensively worked out in both invertebrates and vertebrates, thanks to an ever expanding battery of methods that reveal origins and destinations of axons, and even to some extent of dendrites, cell by cell. Hodology offers a multitude of comparisons, often complicated by a problem peculiarly serious at this level. That is the problem of what criteria are adequate for establishing which cell group in one family or order is equivalent—preferably homologous—to a cell group in another taxon. Besides the simple list of connections in and out of every structure, some significant general features of comparison are opportune. How do two taxa compare in the number of connections between higher and lower brain levels, ascending and descending, between regions at the same level (e.g., corticocortical), between cells of the same local region (often called interneurons or intrinsic neurons), and how localized are the terminations?

2.4 Identifiable Neurons

Widespread among invertebrate phyla and present to a limited extent in anamniote vertebrates is the phenomenon of identifiable neurons. These are neurons that can be recognized and named as the equivalent cell in each individual examined, hence one-of-a-kind cells, most often duplicated on left and right sides. Defined by a combination of anatomical and physiological features, especially their afferent and efferent connectivities, the cells with the same name in different individuals typically belong unequivocally to their unique class but are not identical. Identified neurons are conspicuous and common in leeches, probably in some polychaetes, insects, crustaceans, some gastropods, and a few other taxa. Some workers believe that most of the neurons in certain animals, such as the tectibranch gastropod, Aplysia, are potentially identifiable. A small number of identified neurons are known in lampreys and a pair in many teleosts. It is not clear what factors of phylogeny, or life style correlate with their occurrence. The question of intermediate classes of cells has been raised—those cells which belong, not to a class of 1 but 2 or 10 or 100. It is quite plausible that smallish equivalence classes are abundant even in mammals, taking account of all distinguishing features—immunological, dendrological, and especially functionally relevant connectivity. The significance of this notion is that the equivalence classes: (a) are in fact the biologically important kinds of cells in the nervous system; (b) may run into very large numbers—probably far beyond any other organ in the body; and (c) may represent, in principle, one of the best measures of evolutionary advancement, defined as complexity.

3. Cellular Processes And Messengers

The breakthrough of Hodgkin and Huxley gave us two specific ion channels with distinct roles. Simplifying history, Hagiwara added calcium channels in some tissues of some species. Today we have scores of distinct channels and no clear picture of their distribution among cell types or animal species. It appears not to be the case that a wide array of different channels was evolved only in later, more derived or more complex animals. Studies on relatively primitive living groups show a high diversity of channels. It is still possible that general principles will emerge relating the relative abundance of different kinds of channels—their sensitivities, dynamics, and inter-play—in different kinds of excitable cells and then among the taxa.

Much the same seems to be true for transmitters, modulators, and intracellular messengers. The half dozen or so transmitters, a rather stable list, are each quite widespread among phyla and differences in distribution are mainly be-tween functional systems within a given brain. Modulators are increasing in number; currently there are scores. Several are known to be widespread but no simple picture is yet tenable as to evolution or distribution, particularly if we ask for evidence of what the compounds do neurally.

4. Mesoscopic Traits And/organization

If the vast differences between brains of simpler invertebrates and complex mammals are not obviously correlated with vast differences in the membrane and cellular machinery, could sheer numbers of cells and connections explain complexity? Multiple sources of evidence argue against this as adequate, even though mere numerosity doubtless contributes largely. Al-ready mentioned is the domain of the increase, probably many orders of magnitude, in the number of kinds of neurons. Among the differences are permutations of neuronal personality traits that determine the output of a neuron as an integration of its weightings assigned to inputs and their spatiotemporal patterns and its own proclivities. Lists of integrative variables, each with a spectrum of possible states, run to well over 50 and new items continue to be discovered, such as the recently documented supralinear summation of multiple synaptic inputs upon dendritic gain mediated by an ‘inward-rectifier’ potassium current in leech pagoda cells (Wessel et al. 1999). Differentiation not only of kinds of cells but of assemblies, columns, and circuits appears to have resulted in emergent systems, and these in higher levels of systems. Between the microscopic, cellular, and subcellular levels of many components and interactions and the realm of human achievements, such as recognizing a national political opportunity, there are layers of mesoscopic organization that embody the main variety of evolutionary novelties in the grades of brains and behavior.

This mesoscopic level is where our knowledge of comparative neuroscience is weakest. We lack the advantages of lower, cellular levels where the component elements, structures, and interactions are extensively known in well-studied species. The higher behavioral levels are more difficult to compare but at least provide many measurable variables, just because of their familiarity. The mesoscopic levels that hide the first-order explanations lack both of these advantages and lack even a recognized list of relevant measurable variables. As examples, to suggest the wealth of potential discoveries as well as their slipperiness, one thinks of electrical signs of assembly activity—brain waves, evoked and event-related potentials, sleep stages, seizure stages, patterns of cortical coherence during several kinds of thinking, localized increase in blood flow or oxygen consumption during subtle cognitive states, clinical observations of blindness to animate objects or denial of one’s own left side after local lesions, and ‘magic bullets’ represented by neuroactive molecules that ameliorate clinical depression or obsessive-compulsive disorder. The comparative dimension will surely yield valuable perspectives to this level of analysis.

5. Discriminable Stimuli, Responses, And States

Any overall comparison or estimate of the degree of complexity of the nervous system as a whole, including special adaptations to a particular life style, must take the whole ethogram into account, particularly the range and variety of discriminable social situations, sign stimuli, food, enemy, habitat, and microclimatic signals, plus the range and variety of behavioral responses and internal states. The last named stand for the conative states of readiness, biases, changes of weightings, drives, and moods. The obvious difficulty of enumerating, even of discerning all of these—each representing a theoretically distinguishable spatiotemporal neural pattern—is no reason to neglect their recognition.

Even this list may allow us to forget a major measure of the capacity of the nervous system—one which is hardly touched in the bulk of the literature on comparative behavior and cognition. That is, the extent and depth and detail of the knowledge that an organism can acquire, retrieve, and use in its lifetime. This, like most of the foregoing list, may not be the task of the neuroscientist but comparative neuroscience should be based on the most complete eth-ology. In other words, it embraces neuroethology at every level up to the most subtle behavioral and cognitive abilities.

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