Comparative Neuroanatomy Research Articles

Primate Numerical Competence: Contributions Toward Understanding Nonhuman Cognition

Nonhuman primates represent the most significant extant species for comparative studies of cognition, including such complex phenomena as numerical competence, among others. Studies of numerical skills in monkeys and apes have a long, though somewhat sparse history, although questions for current empirical studies remain of great interest to several fields, including comparative, developmental, and cognitive psychology; anthropology; ethology; and philosophy, to name a few. In addition to demonstrated similarities in complex information processing, empirical studies of a variety of potential cognitive limitations or constraints have provided insights into similarities and differences across the primate order, and continue to offer theoretical and pragmatic directions for future research. An historical overview of primate numerical studies is presented, as well as a summary of the 17‐year research history, including recent findings, of the Comparative Cognition Project at The Ohio State University Chimpanzee Center. Overall, the archival literature on number‐related skills and counting in nonhuman primates offers important implications for revising our thinking about comparative neuroanatomy, cross‐species (human/ape) cognitive similarities and differences, and the evolution of cognition represented by the primate continuum.

Primate numerical competence: contributions toward understanding nonhuman cognition

Nonhuman primates represent the most significant extant species for comparative studies of cognition, including such complex phenomena as numerical competence, among others. Studies of numerical skills in monkeys and apes have a long, though somewhat sparse history, although questions for current empirical studies remain of great interest to several fields, including comparative, developmental, and cognitive psychology; anthropology; ethology; and philosophy, to name a few. In addition to demonstrated similarities in complex information processing, empirical studies of a variety of potential cognitive limitations or constraints have provided insights into similarities and differences across the primate order, and continue to offer theoretical and pragmatic directions for future research. An historical overview of primate numerical studies is presented, as well as a summary of the 17-year research history, including recent findings, of the Comparative Cognition Project at The Ohio State University Chimpanzee Center. Overall, the archival literature on number-related skills and counting in nonhuman primates offers important implications for revising our thinking about comparative neuroanatomy, cross-species (human/ape) cognitive similarities and differences, and the evolution of cognition represented by the primate continuum.

Giuseppe Sterzi (1876-1919) of the University of Cagliari: a brilliant neuroanatomist and medical historian.

irst of all, let me explain why weare now writing about Sterzi.Approximately two years ago I(A.R.) received a message from Prof.Colin Wendell Smith, the secretary ofthe FCAT, who happens to live in theantipodal (for me) island of Tasma-nia, asking me if I could find him thearticle on subcutaneous tissue writtenby an Italian professor named Sterzi.This article had been mentioned byProf. DiDio during one FCAT meetingand Prof. Wendell Smith had alreadyunsuccessfully tried to obtain it viathe usual library system. Since I wasaware that Sterzi had been one of mypredecessors in the Anatomy Chair inCagliari, it was easy for me to send acopy of the article to Prof. WendellSmith, who was surprised to hear thatSterzi had been working in the antip-odal (for him) island of Sardinia andso was indirectly associated with me.In order to provide him with an En-glish summary, I had to read the 172-page article myself. I was greatly im-pressed by the rigorous discussion ofprevious reports and by the amount ofnew findings obtained also through acomparative anatomical/embryologi-cal approach. Prompted by this, webecame interested in Sterzi’s life andscientific achievements, being mani-fest that the studies on the subcutane-ous tissue and some others such asthat on the endolymphatic sac,though important and superbly car-ried out, had been just a parenthesisin his production devoted almost ex-clusively to neuroanatomy and thehistory of anatomy. Favaro (1921)maintains, in fact, that Sterzi madethem mainly to show his critics thathis production was not monothe-matic.

Comparative and correlative neuroanatomy for the toxicologic pathologist.

Xenobiotic-induced neuroanatomic alterations are always regarded as adverse and are commonly used to define reference doses to manage neurotoxic risk. Thus, the neuropathologist plays an essential role in evaluating potential neurotoxicants. The pathologist must be able to recognize the morphologic differences that exist among species, strains, and ages or between genders (comparative neuroanatomy) and to grasp the impact of structural damage on neural function (correlative neuroanatomy). Brain anatomy and function may be used to group the mammals used in neurotoxicity bioassays into 3 classes: rodent, carnivore, and primate. Neural function may or may not be affected by the structural divergence. Rodents are preferred for neurotoxicity assays because their reduced body size allows optimal perfusion at little cost and their smaller brain size permits screening of multiple regions using few sections. However, care must be exercised when interpreting rodent neuropathology data because the rodent paleocortex does not recapitulate the sophisticated neocortical circuitry and functions of carnivores and primates. Knowledge of the neuroanatomic variations that exist among test species assists the neuropathologist in defining the relevance of structural alterations, the potential clinical sequelae of such findings, and the possible significance of similar changes in humans.

Field homology: a meaningless concept.

Most biological homologues involve comparison of single characters in two or more taxa. It is possible, however, to recognize homologous characters between two or more taxa that involve the transformation of one character into many characters or many characters into one character. This type of homology is recognized as field homology and it has been widely used in comparative neuroanatomy. The emergence of the cladistic analysis of embryonic stages in the development of neural characters, however, strongly suggests that field homology is a meaningless concept. When it appears necessary to recognize field homologues, it is because comparisons are being made at an inappropriate level within a given biological hierarchy. Furthermore, recognition of field homologues restricts evolutionary mechanisms to a single mechanism of parcellation as defined by Ebbesson.

The gospel of the fossil brain: Tilly Edinger and the science of paleoneurology

Tilly Edinger (1897–1967) was a vertebrate paleontologist interested in the evolution of the central nervous system. By combining methods and insights gained from comparative neuroanatomy and paleontology, she almost single-handedly founded modern paleoneurology in the 1920s while working at the Senckenberg Museum in Frankfurt am Main. Edinger’s early research was mostly descriptive and conducted within the theoretical framework of brain evolution formulated by O. C. Marsh in the late 19th century. Nevertheless, she became immediately known in 1929 after publishing an extensive review on “fossil brains.” Reconstructing evolutionary history from the fossil record instead of from the comparative analysis of living forms allowed her to identify the sequence of neural innovations within several mammalian lineages. Anti-Jewish terrorism forced Edinger to leave Nazi Germany in 1939. After finding refuge first in England, she continued her career at Harvard’s Museum of Comparative Zoology. There she documented the occurrence of gross neural correlates of specialized behavior in several vertebrate lineages, and identified parallel evolution in mammalian sulcation patterns. Her insight that neural innovations need not be “correlated” with either non-neural innovations or with evolutionary “success” led her to reject Marsh’s theory of progressive increase in brain size over time and other “anthropocentric” understandings of brain evolution. Edinger’s research, her insistence on a stratigraphic and evolutionary framework for interpretation, and her massive compilations of paleoneurological literature established her as the leading definer, practitioner, and chronicler of her field.

What Makes the Human Brain Different?

Despite decades of research that has revolutionized the neurosciences, efforts to explain the major features of human brain evolution are still mostly based on superficial gross neuroanatomical features (e.g. size, sulcal patterns) and on theories of selection for high-level functions that lack precise neurobiological predictions (e.g. general intelligence, innate grammar). Beyond its large size we still lack an account of what makes a human brain different. However, advances in comparative neuroanatomy, developmental biology, and genetics have radically changed our understanding of brain development. These data challenge classic ideas about brain size, intelligence, and the addition of new functions, such as language, and they provide tools with which we can test hypotheses about how human brains diverge from other primate brains.

Comparative vertebrate neuroanatomy: evolution and adaptation

Partial table of contents: EVOLUTION AND THE ORGANIZATION OF THE CENTRAL NERVOUS SYSTEM. Evolution and Variation. Neurons and Sensory Receptors. The Vertebrate Central Nervous System. Theories of Brain Evolution. THE SPINAL CORD AND HINDBRAIN. The Spinal Cord. Sensory Cranial Nerves. Motor Cranial Nerves. The Reticular Formation. The Cerebellum. THE MIDBRAIN. Overview of the Midbrain. Isthmus. Tegmentum and Tori. Optic Tectum. THE FOREBRAIN: DIENCEPHALON. Overview of the Forebrain. Epithalamus. Dorsal Thalamus. THE FOREBRAIN: TELENCEPHALON. Striatum. Dorsal Pallium. Visual Forebrain in Amniotes. Limbic Telencephalon. CONCLUSION. Evolution of the Brain in Vertebrates. Appendix. Glossary. Index.

A forest of principles

I am astonished at Lewis Wolpert's claim that all the big principles in biology are understood — especially in developmental biology. If one knew all the principles then new facts would simply slot into their expected places, as they do in any well understood aspect of physics. But in all areas of biology bewildering new facts are discovered at an increasing rate. I frankly do not believe that Wolpert has a conceptual scheme where each new fact simply evokes an acquiescent nod of the head. Either he is goading us into protest or his ‘principles’ are very different from mine.What can we expect of principles in biology? Consider ‘the principle of quasi-optimal design.’ There are physical limits that dictate the relative sizes of parts of different-sized animals. Thus, a mouse's eye is many times larger than an elephant eye scaled down in proportion to the size of the mouse: the latter would have a minute pupil giving appalling spatial resolution and admitting very little light. Similarly, the elephant's legs would break every time it stood up if they were simply the mouse's legs scaled up in size.These ‘design principles’ are our minds' generalization from particular instances that have been embodied in genomes under the action of natural selection. We have successfully found a few such generalizations, but we emphatically do not understand all the physical limiting factors that have moulded the genomes of all species, and I have not even heard mention of limiting factors in development, although they must surely exist.Now consider a problem in neuroscience. The neocortex of the brain is large in primates and huge in humans; comparative neuroanatomists have told us that it stores knowledge of the world, and if they are right, we can understand the selective advantage it gives us. Neurophysiologists, on the other hand, tell us how the neocortex represents sensory stimuli but say nothing about how this representation is analysed, stored, accessed or used. Only a fool could hold that no new principles might emerge from reconciling these two astonishingly different accounts.I think my examples illustrate the general nature of biological principles. There are not just a few universal ones like the great conservation laws of physics. Instead, they form a forest, and quasi-optimal design is but one tree in it — or perhaps just a branch of the Tree of Adaptation. Wolpert might claim that adaptations are all examples of a single general principle which we already know, but this is unhelpful because we need to know what factor is limiting in each particular case: optics will not help you to understand the elephant's leg bones or neocortical size. If we did understand all the relevant limiting factors, we would be closer to knowing why a species has evolved to a certain average size, why the mass of its neocortex is a particular fraction of its body mass, and so on for many questions that we do not yet even know enough to ask. It is an absolutely safe bet that there are many new principles waiting to be found.Mendel discovered both a whole range of new facts and the principle by which they could be understood, but few are so lucky nowadays. Thus, my request to the good fairy godmother of science would be “Please give me exact references to some facts that require new concepts for their understanding”. I would add “Please pick facts pointing to concepts appropriate for my energies and abilities; I could not handle a tree of Darwinian or Mendelian size, but I would greatly enjoy some of the conceptual fruit still to be found in plenty out among the leafy branches of the Biological Forest of Principles”.

Franz Joseph Gall: Genius or charlatan?

In the popular imagination, the status of Franz Joseph Gall (1758–1828) as charlatan extraordinaire remains secure: a man who could purportedly diagnose differential talent, skill, and personality on the basis of ‘bumps’ on the skull might indeed seem to deserve a place with the tabloid horoscope constructors. Nonetheless, both in his own day and in the view of later historians. Gall was seen as a supreme technician who made lasting contributions to our knowledge of comparative neuroanatomy. In like fashion, his reputation as a revolutionary neuropsychologist continued to be decisive in the development of modern accounts of functional localisation within the human brain. More recently, the significance of Gall's attempt to overthrow classical faculty theory has been widely acknowledged; the terms of current theoretical debate on the modularity of mind were established by Gall. There is, however, one aspect of Gall's work that has not been subject to re-evaluation by the neuroscience community. Gall's ‘sociobiology’ (to phrase the matter somewhat anachronistically) has remained the province of historians. When members of the phrenological movement combined brain anatomy with physiognomy, one of their aims was to address ethical and political issues: masks of the famous and the infamous constituted vivid reminders of law and disorder. Collections of early phrenological portraits, one of which is described in the following paper [Kaufman, M.H. and Shaw, J.P. Some interesting portraits from the history of phrenology which were probably used to illustrate lectures on physiognomy. Journal of Neurolinguistics 8, 295–305. 1994], were likewise designed to illustrate how the interaction of intellectual and affective powers determined the individual's contribution to society. Such collections are a prime resource in our (as yet inadequate) attempts to understand how the nineteenth century set the agenda for twentieth century psychology and neuroscience.

Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds

Song and brain structure are compared amongst 41 species of oscine birds by using the method of independent evolutionary contrasts. We find a significant correlation between the relative volume of the song control centre, the high vocal centre (HVC), and the number of song types typically found in the repertoire. Relative HVC volume is not correlated with the number of different syllable types per song bout. The relative volume of a second song nucleus, area X, is not significantly correlated with either measure. Relative HVC volume is uncorrelated with relative volume of the hippocampus, a brain area involved in other forms of memory. This is the first evidence for repeated independent evolution of an association between complexity of learned song and the relative volume of one of the song control nuclei though to be involved in song learning.

Paedomorphosis and Simplification in the Nervous System of Salamanders; pp. 153–161

Comparative neuroanatomists since Herrick [1914] have been aware of the paradox that the brain of amphibians, especially salamanders, is less complex than one would expect based on their phylogenetic position among the Tetrapoda. Many features of the brain are less differentiated in salamanders than in tetrapod outgroups, including chondrichthyans and bony fishes, and for some brain characters, the salamander brain is even more simple than that of the agnathans. Here, we perform a cladistic analysis on 23 characters of four sensory systems (visual, auditory, lateral line and olfactory) and the brain. Our taxa include myxinoids, lampreys, chondrichthyans, actinopterygians, Latimeria, Neoceratodus and the Iepidosirenid lungfishes, amniotes, frogs, caecilians, salamanders and bolitoglossine salamanders. Of the 23 characters we examined, 19 are most parsimoniously interpreted as secondarily simplified in salamanders from a more complex ancestral state, two characters are equally parsimonious under both hypotheses, one character (well developed ipsilateral retinotectal projections) is more complex in bolitoglossine salamanders than in vertebrates generally, and only one character (migration of neurons in the medial pallium) is most parsimoniously interpreted as retention of the plesiomorphically simple condition. Secondary simplification of the salamander brain appears to result from paedomorphosis, or retention of juvenile or embryonic morphology into adulthood. Paedomorphosis is correlated with an increase in genome size, which in turn is positively correlated with cell size, but negatively correlated with cell proliferation and differentiation rates. Available data suggest that, although increasing genome size and paedomorphosis tend to compromise the function of the salamander brain, compensating mechanisms have evolved that may restore or even enhance brain function.

Paedomorphosis and Simplification in the Nervous System of Salamanders; pp. 162–170

Comparative neuroanatomists since Herrick [1914] have been aware of the paradox that the brain of amphibians, especially salamanders, is less complex than one would expect based on their phylogenetic position among the Tetrapoda. Many features of the brain are less differentiated in salamanders than in tetrapod outgroups, including chondrichthyans and bony fishes, and for some brain characters, the salamander brain is even more simple than that of the agnathans. Here, we perform a cladistic analysis on 23 characters of four sensory systems (visual, auditory, lateral line and olfactory) and the brain. Our taxa include myxinoids, lampreys, chondrichthyans, actinopterygians, Latimeria, Neoceratodus and the Iepidosirenid lungfishes, amniotes, frogs, caecilians, salamanders and bolitoglossine salamanders. Of the 23 characters we examined, 19 are most parsimoniously interpreted as secondarily simplified in salamanders from a more complex ancestral state, two characters are equally parsimonious under both hypotheses, one character (well developed ipsilateral retinotectal projections) is more complex in bolitoglossine salamanders than in vertebrates generally, and only one character (migration of neurons in the medial pallium) is most parsimoniously interpreted as retention of the plesiomorphically simple condition. Secondary simplification of the salamander brain appears to result from paedomorphosis, or retention of juvenile or embryonic morphology into adulthood. Paedomorphosis is correlated with an increase in genome size, which in turn is positively correlated with cell size, but negatively correlated with cell proliferation and differentiation rates. Available data suggest that, although increasing genome size and paedomorphosis tend to compromise the function of the salamander brain, compensating mechanisms have evolved that may restore or even enhance brain function.

Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous voles

In the present work we evaluated the degree of sexual dimorphism in two cell groups of the medial preoptic-anterior hypothalamus (MPOA-AH) in monogamous and polygamous voles. Quantitative determinations were made of volume, cell number, and cell density for the anteroventral-periventriular nucleus (AVPV) and the sexually dimorphic nucleus of the preoptic area (SDN-POA). Polygamous montane voles ( Microtus montanus) had a greater degree of sexual dimorphism in both cell groups than did monogamous prairie voles ( M. ochrogaster). Most notable was the complete absence of the AVPV in male montane voles; male montane voles also had a significantly larger SDN-POA volume than did females. The only sexual dimorphism in prairie voles was a greater cell density in the female AVPV. In addition, prairie voles had larger relative brain size than did montane voles. Comparative behavioral studies have revealed a correlation between the degree of sexual dimorphism in external morphology and mating system, i.e., polygamous species display greater levels of dimorphism than do monogamous species. The present results indicate that the effects of sexual selection can also be seen in those brain regions, like the hypothalamus, that underlie social and reproductive behavior. Moreover, these results support the hypothesis that neuroanatomic dimorphisms in the MPOA-AH may be related to sex differences in behavior.

Homology and Evolutionary Origins of the 'Neocortex'

The telencephalon of mammals is characterized by the presence of a hexalaminated structure on its external surface, with specific auditory, visual, somatosensory and motor regions. Due to its seeming unique presence in mammals, it is frequently designated as the neocortex. The evolutionary origins of the so-called neocortex have long puzzled comparative neuroanatomists, in view of the seeming absence of a neocortical-like anlage in nonmammalian amniotes. The resolution of this puzzle requires analysis of both adult and embryonic brains. Experimental neuroanatomical, physiological and behavioral methods applied to adult avian and reptilian brains have finally clarified several fundamental questions regarding the origins of 'neocortex' and have indicated that these origins can be viewed as consequent to two separate events: (1) The elaboration of constituent neuronal populations and their associated connections that are common to the telencephalae of both nonmammalian and mammalian amniotes. In mammals these populations are found within the so-called neocortex. In birds and reptiles, most of these neurons are found within the dorsal and dorsolateral ventricular ridges (DVR and DLVR). (2) In mammals, the components of the DVR and DLVR are incorporated into the thin overlying pallium to form a laminated 'neocortex'. Analysis of development in domestic chicks suggests that the DVR is one of several prosencephalic neuromeres ('Prosomeres') that contribute to the ontogeny of comparable structures in birds. Perhaps in mammals, as well, cortical development is consequent to incorporation of these several prosomeres into proliferative ependyma of the pallial mantle.

Comparative neuroanatomy of the histaminergic system in the brain of the frog xenopus laevis

The distribution of the histaminergic neuronal system in the brain of the clawed frog Xenopus laevis was mapped with an antiserum against carbodiimide-fixed histamine and compared to that in mammals. The histamine-immunoreactive cell bodies were located in a small area of the posterolateral hypothalamus, close to the dorsal infundibular nucleus, which contains catecholaminergic and serotonergic neurons. This area may be homologous to the tuberomammillary nucleus in mammals. A thick process extended from each cell between the ependymal cell layer and terminated in the ventricle lumen. The number of histaminergic cell bodies in adult Xenopus brain was relatively low, as compared with the mammalian brain. Preliminary analysis of adjacent sections stained with antisera against GABA or serotonin indicated that the histamine cells were not immunoreactive for these. The pathways and distribution of histaminergic fibers in Xenopus brain showed many similarities to mammals. The densest fiber networks were present in the medial basal forebrain, particularly in the medial amygdala and septum. A distinct cluster of fibers was concentrated around the cell bodies of nucleus accumbens. In most pallial areas, the density was moderate to low. In the primordial piriform cortex and the striatum, very few fibers were seen. In diencephalon, highest fiber densities were found in the anterior and ventral thalamus and posterior and lateral hypothalamus. In hindbrain, the density was highest in the medullary central gray, as in some mammals. The results suggest that the general pattern of the histaminergic system in vertebrate brain is conserved from amphibians to mammals.

Comparative neuroanatomy: foundations for a comparative neurobiology

Comparative neuroanatomy: foundations for a comparative neurobiology

Some observations on the cerebellopontine projections in the cat - with a hypothesis to explain species differences

The projection from the lateral and interposed nuclei of the cerebellum to the pons was investigated by means of autoradiography of anterogradely transported tritiated leucine. Dense termination, in part of axo-somatic nature, was observed in clusters within the central part of the nucleus reticularis tegmenti pontis. Termination in the pontine nuclei proper was found in small clusters directly ventral to the medial lemniscus and in trace-like amounts in the paramedian subnucleus. The results are discussed in relation to ponto-cerebellar circuits and comparative neuroanatomy.

Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon

Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon

The discovery, proof and reproof of neurosecretion (Speidel, 1917; Scharrer and Scharrer, 1934).

Seventeen years before the Scharrers demonstrated neurosecretory activity of neurons within the brains of vertebrates and invertebrates and convinced the scientific world of the existence of a neuroendocrine system, Carl Caskey Speidel (1917) had identified glandular neurons in the spinal cord of the skate, postulated a neurosecretory function, and performed experiments to prove his hypothesis. The correct conclusions that he formulated from morphologic observations were not believed by biologists until 'proved' by the Scharrers, who acknowledged his pioneering contributions. The Scharrers studied many species and even demonstrated neurosecretion in nemertine worms, now believed to be closely related to the ancestors of all vertebrates. Evolutionary theorists had speculated on neuroglandular function as early as 1900, and the contribution of comparative neuroanatomists to this field have resulted in a major medical advance.