Sven O. E. Ebbesson

The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity

SummaryRecently discovered neocortical equivalents in anamniotes and certain patterns of interspecific variability in brain organization provide new insights into evolutionary and ontogenetic mechanisms of development. The new data suggest that nervous systems become more complex, not by one system invading another, but by a process of parcellation that involves the selective loss of connections of the newly formed daughter aggregates and subsystems. The parcellation process is reflected in the normal ontogenetic development of the CNS in a given species and can be manipulated, to a certain extent, by deprivation or surgically induced sprouting.The parcellation theory allows certain predictions about the range of variation of a given system at all levels of analysis including the cellular and aggregate levels. For example, the interspecific variability in organization of cortical columns, thalamic nuclei, cortical areas and tectal layers can be explained. The findings, summarized here, suggest that diffuse, undifferentiated systems existed in the beginning of vertebrate evolution and that during the evolution of complex behaviors, and analytical capacities related to these behaviors, a range of patterns of neural systems evolved that relate to these functions. One principle underlying the growth, differentiation and multiplication of neural systems appears to be the process of parcellation as defined by the theory.

Projections to the midbrain tectum in Salamandra salamandra L.

SummaryFollowing unilateral iontophoretic application of HRP into the optic tectum of Salamandra salamandra, retrogradely HRP-filled cells were found bilaterally in the pretectum, tegmentum isthmi, the reticular formation, pars medialis, and in the nucleus vestibularis magnocellularis. The area octavo-lateralis projects only to the caudal part of the tectum. Ipsilateral projections were noted from the dorsal gray columns of the cervical spinal cord, the dorsal tegmentum, the thalamus dorsalis pars medialis, thalamus dorsalis, pars anterior (to the rostral one-third of the tectum), the thalamus ventralis (in its entire rostro-caudal extent), and the preoptico-hypothalamic complex. Retrogradely filled cells were identified in deeper layers of the contralateral tectum. There are two telencephalic nuclei projecting ipsilaterally to the tectum via the lateral forebrain: the ventral part of the lateral pallium, and the posterior strio-amygdalar complex.

Connections of the olfactory bulb in the piranha (Serrasalmus nattereri)

SummaryThe connections of the olfactory bulb were studied in the piranha using the Nauta and horseradish-peroxidase methods. Three olfactory tracts project to seven terminal fields in the telencephalon and one in the diencephalon, all of them bilaterally. The contralateral olfactory bulb also receives a small input. All contralateral projections decussate in the anterior commissure and are relatively weak compared to the ipsilateral projections. HRP-containing cells were found in all of the ipsilateral telencephalic aggregates receiving an olfactory tract projection; the contralateral side was free of labeled cell bodies. Although only about one fourth of the entire telencephalon receives a direct olfactory input, the high degree of differentiation of the olfactory system suggests that the piranha depends substantially on the sense of olfaction and that this species may be a good model for further studies on olfactory mechanisms.

Organization of ascending spinal projections in Caiman crocodilus

SummaryAscending spinal projections in the caiman (Caiman crocodilus) were demonstrated with Nauta and Fink-Heimer methods following hemisections of the third spinal segment in a series of twelve animals. These results were compared with earlier data in the literature obtained from a turtle, a snake, and a lizard using the same experimental and histological procedures. The results show remarkable similarities considering that each species represents a different reptilian order with different evolutionary history and habitat. However, the caiman displays several important peculiarities.Although the dorsal funiculus of the caiman contains the largest number of ascending spinal projections of the four species examined, this funiculus has not differentiated into cuneate and gracile fasciculi as is the case in the tegu lizard. The ventro-lateral ascending spinal projections follow a fundamentally similar general morphologic pattern in the four species with only minor variations. The anatomical arrangement in the caiman and tegu lizard appears most similar in the high cervical and the medullary regions; however, this is not the case in midbrain and thalamic regions where considerably more extensive projections are seen in the caiman. In the caiman an extensive spinal connection to the ventro-lateral nucleus of the dorsal thalamus is present; this connection is reminiscent of the mammalian spinal projection to the ventro-basal complex. The caiman has in common with the other three reptilian species a small projection to another dorsal thalamic region that is apparently homologous to the mammalian intralaminar nuclei, which are the destination of the mammalian paleospinothalamic tract.

Retinofugal and retinopetal connections in the upside-down catfish (synodontis nigriventris).

SummaryThe retinofugal and retinopetal connections in the upside-down catfish Synodontis nigriventris were studied by use of the horseradish-peroxidase (HRP) techniques, autoradiography, and degeneration-silver methods. An unusual retinal projection to the torus semicircularis as well as projections to the retina from three different sources in the brain are described. After intra-ocular injections of HRP, labeled cells were found in the optic tectum, the dorsomedial optic nucleus and one of the pretectal nuclei. These new findings support the basic hypothesis (i) that neuronal connections are more extensive in primitive brains, and (ii) that the evolutionary development of more complex brains involves the loss of some selected connections.

An ‘on the slide’ modification of the De Olmos-Heimer horseradish peroxidase method

The De Olmos-Heimer horseradish peroxidase method has been simplified without losing its sensitivity. The modification involves the use of cryostat sections and omitting several steps from the original procedure. The modification is especially suitable for small pieces of tissue that would otherwise require imbedding.

Terminal distribution of retinal fibers in the tegu lizard (Tupinambis nigropunctatus)

SummaryThe retinal projections in the tegu lizard were traced using degeneration-silver methods. Bilateral projections were found to the dorsolateral geniculate and the posterodorsal nuclei. Unilateral, crossed projections were traced to the suprachiasmatic nucleus, the ventrolateral geniculate nucleus, the mesencephalic lentiform nucleus, nucleus geniculatus praetectalis, the ectomammillary nucleus, and the optic tectum. Some of these connections are distinctly different from those reported in other reptiles and suggest that important interspecific variations occur among reptiles.

Projections of the optic tectum and the mesencephalic nucleus of the trigeminal nerve in the tegu lizard (Tupinambis nigropunctatus).

SummaryFibers undergoing Wallerian degeneration following tectal lesions were demonstrated with the Nauta and Fink-Heimer methods and traced to their termination. Four of the five distinct fiber paths originating in the optic tectum appear related to vision, while one is related to the mesencephalic nucleus of the trigeminus. The latter component of the tectal efferents distributes fibers to 1) the main sensory nucleus of the trigeminus, 2) the motor nucleus of the trigeminus, 3) the nucleus of tractus solitarius, and 4) the intermediate gray of the cervical spinal cord.The principal ascending bundle projects to the nucleus rotundus, three components of the ventral geniculate nucleus and the nucleus ventromedialis anterior ipsilaterally, before it crosses in the supraoptic commissure and terminates in the contralateral nucleus rotundus, ventral geniculate nucleus and a hitherto unnamed region dorsal to the nucleus of the posterior accessory optic tract.Fibers leaving the tectum dorso-medially terminate in the posterodorsal nucleus ipsilaterally and the stratum griseum periventriculare of the contralateral tectum. The descending fiber paths terminate in medial reticular cell groups and the rostral spinal cord contralaterally and in the torus and the lateral reticular regions ipsilaterally. The ipsilateral fascicle also issues fibers to the magnocellular nucleus isthmi.

Multimodal torus in the weakly electric fish Eigenmannia.

1 General Introduction.- 2 General Description of the Torus and Commissural Connections.- 2.1 Introduction.- 2.2 Material and Methods.- 2.3 Results.- 2.4 Discussion.- 2.4.1 Torus Superlamination and the T Unit System.- 2.5 Summary.- 3 Connections with the Posterior Lateral Line Lobe.- 3.1 Introduction.- 3.2 Material and Methods.- 3.3 Results.- 3.3.1 Injections in the Posterior Lateral Line Lobe.- 3.3.2 Injections in the Torus.- 3.3.3 Projections to the Nucleus Praeeminentialis Pars Lateralis and Pars Medialis.- 3.4 Discussion.- 3.4.1 The Posterior Lateral Line Lobe-Toms Loops.- 3.4.2 Possible Roles of Feedback of the Descending Electrosensory Pathway.- 3.4.3 Interconnection of Posterior Lateral Line Lobe and Toral Layers.- 3.4.4 A Temporal Comparator in the Torus.- 3.5 Summary.- 4 Connections with the Mesencephalic Tectum.- 4.1 Introduction.- 4.2 Material and Methods.- 4.3 Results.- 4.3.1 Injections of the Tectum.- 4.3.2 Injections in the Torus.- 4.4 Discussion.- 4.4.1 Vertical Overlap of Inputs with Other Modalities.- 4.5 Summary.- 5 Connections with the Cerebellum.- 5.1 Introduction.- 5.2 Material and Methods.- 5.3 Results.- 5.4 Discussion.- 5.5 Summary.- 6 Connections with the Medial Octavolateralis Complex and with the Reticular Formation.- 6.1 Introduction.- 6.2 Material and Methods.- 6.3 Results.- 6.4 Discussion.- 6.5 Summary.- 7 Concluding Remarks.- 7.1 Organizational Frame of the Torus.- 7.2 Ascending Outputs of the Torus.- References.

Neuroanatomical Implications for Neuroethology

Neuroethology is the science concerned with elucidating the neurophysiological bases of behavioral functions (Ewert, 1980). The methods used in this field range from brain stimulation to single unit recording. Needless to say, such studies depend on a thorough understanding of neuroanatomy, but the relationship between neuroanatomy and neuroethology is more important than that. In fact, I propose that comparative neuroanatomy must be considered an integral part of neuroethology, each giving meaning to the other. The interspecific variability of structures forms the bases for the variability in behavior and neurophysiological interactions. Since most of the contributors to this volume are ethologists and physiologists, I will review some aspects of comparative neuroanatomy that relates specifically to neuroethology. I will deal prinicpally with the evolution of neuroanatomical methods and interspecific variability of brain organization and show how this relates to a new view of evolutionary and ontogenetic plasticity of connections. It is my purpose to show the wonderful potential of integrating the comparative morphological discipline with those of neurophysiology and behavior.