The thalamus as a neuronal oscillator.

The thalamus has long been seen as responsible for relaying information on the way to the cerebral cortex, but it has not been until the last decade or so that the functional nature of this relay has attracted significant attention. Whereas earlier views tended to relegate thalamic function to a simple, machine-like relay process, recent research, reviewed in this article, demonstrates complicated circuitry and a rich array of membrane properties underlying the thalamic relay. It is now clear that the thalamic relay does not have merely a trivial function. Suggestions that the thalamic circuits and cell properties only come into play during certain phases of sleep to effectively disconnect the relay are correct as far as they go, but they are incomplete, because they fail to take into account interesting and variable properties of the relay that, we argue, occur during normal waking behavior. Although the specific function of the circuits and cellular properties of the thalamic relay for waking behavior is far from clear, we offer two related hypotheses based on recent experimental evidence. One is that the thalamus is not used just to relay peripheral information from, for example, visual, auditory, or cerebellar inputs, but that some thalamic nuclei are arranged instead to relay information from one cortical area to another. The second is that the thalamus is not a simple, passive relay of information to cortex but instead is involved in many dynamic processes that significantly alter the nature of the information relayed to cortex.

Functional organization of thalamocortical relays

The afferent projections to the olfactory cortical areas from the olfactory bulb and the prepiriform cortex have been studied in the rat, using the autoradiographic method for demonstrating axonal connections. In order to relate closely the results of these experiments to the structure of the olfactory cortical areas, the cytoarchitectonic characteristics of these areas have also been described.

The olfactory cortical areas, which receive a direct input from the olfactory bulb, include the anterior olfactory nucleus, the ventral portion of the tenia tects, the olfactory tubercle, the prepiriform cortex, the nucleus of the lateral olfactory tract, the cortical amygdaloid nucleus, and the lateral entorhinal area. All of these areas are composed primarily of pyramidal cells and have three basic layers: a superficial plexiform layer containing the apical dendrites of the pyramidal cells (layer I), a pyramidal cell layer (layer II), and a deeper polymorphic cellular layer (layer III). In each area layer I may be divided into a superficial portion (IA) and a deeper portion (IB).

The autoradiographic experiments have shown that all of the olfactory cortical areas receive projections from the prepiriform cortex as well as from the olfactory bulb, and that these two projections have complementary laminar patterns of termination which are the same in every area. Throughout the olfactory cortex the fibers from the olfactory bulb terminate exclusively in layer IA, in relation to the distal segments of the apical dendrite of the pyramidal cells, whereas the fibers from the prepiriform cortex terminate in layer IB, in relation to more proximal segments of the apical dendrites, and also in layer III. The boundary between the two projections within layer I is very sharp, with minimal overlap. In contrast to this precise laminar organization, there is little evidence for a topographical organization within these Projections.

An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex.

The neuropil of the glomeruli of the rat olfactory bulb has been studied with the electron microscope with a view to elucidating the type of processes involved - dendrites, appendages and axons - their cellular identity, and the synaptic relationships they establish. The problems encountered in defining these are considered and criteria based on the previous study of neuron types and on examination of serial sections are put forward. The glomeruli are large structures containing many thousands of processes and are the sole site of termination of the olfactory receptor axons. The terminals of the latter are characteristically electron-dense, allowing identification in normal material; they run through the glomeruli making many synapses by means of spherical vesicles and asymmetrical thickenings on to all types of dendritic profile. The glomerular dendritic arborizations of mitral and tufted cells, which are indistinguishable from each other, start as large, fairly regular, pale profiles but become increasingly varicose as they branch and diminish in size. They regularly show groups of spherical vesicles, often in association with asymmetrical synaptic thickenings directed from the dendrite; these are typically associated with return, reciprocal, synapses of the symmetrical type from profiles containing large flattened vesicles. These latter profiles are those of the dendrites and gemmules of periglomerular cells; the dendrites are of irregular outline and give rise to many appendages, mostly gemmules making synaptic contact with mitral or tufted cell dendrites. A small number of pale axon terminals containing either small or large flattened vesicles, derived from short-axon and periglomerular cells respectively, synapse with symmetrical thickenings on to the periglomerular cell dendritic processes. Close associations of particular types of axo-dendritic and dendro-dendritic synapses on interconnecting processes, termed synaptic patterns, are described and their significance considered. The nature of the glomerular interactions is discussed and then placed in the context of other, smaller glomeruli in the central nervous system; certain common principles of glomeruli are suggested.

The neuropil of the glomeruli of the olfactory bulb.

Presynaptic inhibition in the vertebrate central nervous system.

Optic fibers of retinal origin terminate in the lateral geniculate body exclusively in the so called glomerular synapses. They can be recognized on the basis of their unusually large irregular mitochondria having very few cristae. In the cat the structure of the optic terminal profiles is rather dense. The majority of terminals in most glomeruli originate from axons of other source. Relatively large axon terminal profiles of unusually light structure cannot be brought to degeneration by any interference with extraneous pathways. From Golgi information it becomes obvious that they originate from local Golgi 2nd type neurons. Small rather dense axonal profiles of the glomeruli can occasionally be traced back by degeneration to the occipital cortex (parastriate), although most of the descending cortical afferents of the lateral geniculate body terminate outside the glomeruli on more proximal parts of the dendrites. — Axo-axonic synapses are very frequent. If an optic terminal is involved, it appears that by structural standards it is “presynaptic” to the non optic. As judged, however, from the numerous axoaxonic contacts persisting after enucleation, many of the contacts are established between non optic axon terminals. — The progress of secondary degeneration and particularly the removal from the glomeruli of degeneration fragments is unexpectedly rapid. — The possible functional significance of these findings, especially also with regards to presynaptic inhibition, is discussed.

J. Szentágothai

Papers

Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body