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

Abstract

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 m 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 m, 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, coaxially 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.

Motion detection, noise reduction, texture suppression, and contour enhancement by spatiotemporal Gabor filters with surround inhibition

“…This is a model design issue since the existing electrophysiological studies (Knierim and van Essen 1992;Nothdurft et al 1999) exclude the CRF region from suppression measurements and therefore cannot conclusively answer the question of whether or not suppression originates from the CRF. The results of some anatomic studies on the distribution of horizontal interconnections in area V1 show that the sites (buttons) at which a neuron connects to other neurons are located outside a certain area around the considered neuron (Bosking et al 1997). This may point to exclusion of the CRF area from the surround weighting function.…”

Local networks in visual cortex and their influence on neuronal responses and dynamics

“…There is also intriguing recent data that these horizontal connections, and by extension the map they represent, may influence the spontaneous patterns of cortical activity [4,68]. There is also evidence in tree shrews and monkeys that the extent of the patchy connections may be extended along the retinotopic dimension that reflects the orientation that they represent [11].…”

“…The evidence that these local connections respect the structure of the orientation map is generally lacking. Bulk tracer injections label a dense, homogeneous set of neurons within 500 lm of the injection site [11,28,36]. Individual filled neurons have dendritic arbors that can be seen to cross the boundaries of orientation domains and pinwheel centers [39].…”

“…Unlike previous experiments combining extracellular recordings with optical imaging, the use of intracellular recordings permits the measurement of subthreshold membrane potential, which is much more closely linked to synaptic inputs than the spiking activity of neurons. Anatomical data suggests that a large majority of the synaptic input to V1 neurons is derived from a fairly small patch of surrounding cortex [11,76]. We are therefore in a position to test whether the tuning of the subthreshold membrane potential responses reflects the orientation representation in the local neighborhood.…”

Selective interhemispheric circuits account for a cardinal bias in spontaneous activity within early visual areas

“…There is manifold evidence that neurons in the visual cortex responding to contours of the same orientation are preferentially linked by long-range patchy connections (Gilbert and Wiesel, 1989;Malach et al, 1993;Bosking et al, 1997;Schmidt et al, 1997a;Stettler et al, 2002). A close relationship between the anatomical configuration of that patch system as determined by tracer injections, and the structure of maps acquired through visual stimulation has been suggested (Muir et al, 2011).…”