Introduction to synaptic circuits, Gordon M.Shepherd and Christof Koch membrane properties and neurotransmitter actions, David A.McCormick peripheral ganglia, Paul R.Adams and Christof Koch spinal cord - ventral horn, Robert E.Burke olfactory bulb, Gordon M.Shepherd, and Charles A.Greer retina, Peter Sterling cerebellum, Rodolfo R.Llinas and Kerry D.Walton thalamus, S.Murray Sherman and Christof Koch basal ganglia, Charles J.Wilson olfactory cortex, Lewis B.Haberly hippocampus, Thomas H.Brown and Anthony M.Zador neocortex, Rodney J.Douglas and Kevan A.C.Martin Gordon M.Shepherd. Appendix: Dendretic electrotonus and synaptic integration.

The synaptic organization of the brain

Horizontal connections, formed primarily by the axon collaterals of pyramidal neurons in layer 2/3 of visual cortex, extend for millimeters parallel to the cortical surface and form patchy terminations. Previous studies have provided evidence that the patches formed by horizontal connections exhibit modular specificity, preferentially linking columns of neurons with similar response characteristics, such as preferred orientation. The issue of how these connections are distributed with respect to the topographic map of visual space, however, has not been resolved. Here we combine optical imaging of intrinsic signals with small extracellular injections of biocytin to assess quantitatively the specificity of horizontal connections with respect to both the map of orientation preference and the map of visual space in tree shrew V1. Our results indicate that horizontal connections outside a radius of 500 microm from the injection site exhibit not only modular specificity, but also specificity for axis of projection. Labeled axons extend for longer distances, and give off more terminal boutons, along an axis in the map of visual space that corresponds to the preferred orientation of the injection site. Inside of 500 microm, the pattern of connections is much less specific, with boutons found along every axis, contacting sites with a wide range of preferred orientations. The system of long-range horizontal connections can be summarized as preferentially linking neurons with co-oriented, co-axially aligned receptive fields. These observations suggest specific ways that horizontal circuits contribute to the response properties of layer 2/3 neurons and to mechanisms of visual perception.

Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex

We perceive the visual world as a unitary whole, yet one of the guiding principles of nearly a half century of neurophysiological research since the early recordings by Hartline (1938) has been that the visual system consists of neurons that are driven by stimulation within small discrete portions of the total visual field. These classical receptive fields (CRFs) have been mapped with the excitatory responses evoked by a flashed or moving stimulus, usually a spot or bar of light. Most of the visual neurons, in turn, are organized in a series of maps of the visual field, at least 10 of which exist in the visual cortex in primates as well as additional topographic representations in the lateral geniculate body, pulvinar and optic tectum (Allman 1977, Newsome & Allman 1980, Allman & Kaas 1984). It has been widely assumed that perceptual functions that require the integration of inputs over large portions of the visual field must be either collective properties of arrays of neurons representing the visual field, or features of those neurons at the highest processing levels in the visual system, such as the cells in inferotemporal or posterior parietal cortex that typically possess very large receptive fields and do not appear to be organized in visuotopic maps. These assumptions have been based on the results of the many studies in which receptive fields were mapped with conventional stimuli, presented one at a time, against a featureless background. However, unlike the neurophysiologist's tangent screen, the natural visual scene is rich in features, and there is a growing body of evidence that in many visual neurons stimuli presented outside the CRF strongly and selectively influence neural responses to stimuli presented within the CRF. These results suggest obvious mechanisms for local-global comparisons within visuotopically organized structures. Such broad and specific surround mechanisms could participate in many functions that require the integration of inputs over wide regions of the visual space such as the perceptual constancies, the segregation of figure from ground, and depth perception through motion parallax. In the first section of this paper, we trace the historical development of the evidence of response selectivity for visual stimuli presented beyond the CRF; in the second, examine the anatomical pathways that sub serve these far-reaching surround mechanisms; and in the third, explore the possible relationships between these mechanisms and perception.

Stimulus Specific Responses from Beyond the Classical Receptive Field: Neurophysiological Mechanisms for Local-Global Comparisons in Visual Neurons

A zonal organization of odorant receptor gene expression in the olfactory epithelium

https://www.cell.com/neuron/pdf/S0896-6273(00)80803-X.pdf

Optical imaging of odorant representations in the mammalian olfactory bulb.

The projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis) have been analyzed with anterograde degeneration and autoradiographic methods for identifying axonal projections, and with the horseradish peroxidase method for identifying the distribution of neurons from which these projections originate. The cytoarchitectonic features of the paleocortical areas which receive projections from the main and the accessory olfactory bulb have also been described. The efferent projections of the accessory olfactory bulb are distributed to the bed nucleus of the accessory olfactory tract, the medial amygdaloid area, the posteromedial cortical amygdaloid area, and to the caudal portion of the bed nucleus of the stria terminalis. In contrast, the efferent projections of the main olfactory bulb are distributed to the anterior olfactory nucleus, the tenia tecta, the olfactory tubercle, the pyriform cortex, the anterior cortical amygdaloid area, the posterolateral cortical amygdaloid area, and to the lateral entorhinal cortex. These observations are consistent with the notion that the olfactory system can be divided into at least two major subsystems: one related to the vomeronasal organ and accessory olfactory bulb, and another related to the main olfactory organ and main olfactory bulb. The paleocortical areas receiving olfactory projections have three basic layers: a superficially positioned plexiform layer (layer I), a pyramidal cell layer (layer II), and a polymorphic cell layer (layer III). The projections of both the main and the accessory olfactory bulb terminate in the outer portion of the plexiform layer (sublamina Ia). Sublamina Ia contains the distal segments of dendrites which originate from a heterogeneous population of neurons located in layer II and, to a lesser extent, layer III. Although the efferent projections of the main and the accessory olfactory bulb are segregated, evidence for a more refined topographical organization within these projections was not obtained. However, the distribution of retrogradely labeled neurons in the main olfactory bulb, following injections of horseradish peroxidase into its various paleocortical targets, indicates that the olfactory projections to these areas may not all originate from the same population of cells.

Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis).

Odor-induced patterns of deoxyglucose consumption in the olfactory bulb of the tree shrew,Tupaia glis

The topographic organization of the orientation column system in the tree shrew striate cortex was examined by using 2-deoxyglucose autoradiography to map the cortical sites of increased metabolic activity produced by visual stimulation with stripes of a single orientation. Awake experimental tree shrews (freely moving, restrained, or paralyzed) were given injections of deoxyglucose label and then stimulated with vertical, horizontal, or oblique stripes for 45--75 min. Autoradiographs of coronal sections through the striate cortex revealed regularly spaced radial zones of increased deoxyglucose uptake 150--350 micrometers wide, extending from the cortical surface to the white matter, separated by interzone regions of lower uptake. The radial zones were most densely labeled and distinct in layers I--IIIb and least distinct in layer IV, which was continuously and densely labeled throughout both the radial zone and interzone regions. These radial zones, which were not present in control animals that viewed many orientations, reflect the locations of cortical cells activated by a single stimulus orientation. Reconstructions of the radial zones from serial sections produced maps of the distribution of increased deoxyglucose uptake across striate cortex. The maps reveal a highly organized system of narrow, parallel bands that are slightly wavy and have a mean spacing of 530 micrometers. The band pattern was confirmed in sections cut tangential to the cortical surface and was similar in animals stimulated with either vertical or horizontal stripes; the bands consistently abut the 17--18 border at nearly right angles and extend across the striate cortex in a generally posteromedial direction. These patterns of increased deoxyglucose consumption confirm the anisotropic distribution of orientation-selective cells across the tree shrew striate cortex, suggested in the preceding microelectrode study (Humphrey and Norton, '80). The density distribution of label within the bands further suggests that the anisotropy is due to a system of parallel, somewhat wavy iso-orientation lines arranged roughly perpendicular to the 17--18 border.

Leslie C. Skeen

Papers

Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis).

Odor-induced patterns of deoxyglucose consumption in the olfactory bulb of the tree shrew,Tupaia glis

Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping.

Deoxyglucose mapping of the orientation column system in the striate cortex of the tree shrew, Tupaia glis.