Simple cells within layer IV of the cat primary visual cortex are selective for lines of a specific orientation. It has been proposed that their receptive-field properties are established by the pattern of connections that they receive from the lateral geniculate nucleus (LGN) of the thalamus. Thalamic inputs, however, represent only a small proportion of the synapses made onto simple cells, and others have argued that corticocortical connections are likely to be important in shaping simple-cell response properties. Here we describe a mechanism that might be involved in selectively strengthening the effect of thalamic inputs. We show that neighbouring geniculate neurons with overlapping receptive fields of the same type (on-centre or off-centre) often fire spikes that are synchronized to within 1 millisecond. Moreover, these neurons often project to a common cortical target neuron where synchronous spikes are more effective in evoking a postsynaptic response. We propose that precisely correlated firing within a group of geniculate neurons could serve to reinforce the thalamic input to cortical simple cells.

A recent computational theory suggests that visual processing in the retina and the lateral geniculate nucleus (LGN) serves to recode information into an efficient form (Atick and Redlich, 1990). Information theoretic analysis showed that the representation of visual information at the level of the photoreceptors is inefficient, primarily attributable to a high degree of spatial and temporal correlation in natural scenes. It was predicted, therefore, that the retina and the LGN should recode this signal into a decorrelated form or, equivalently, into a signal with a "white" spatial and temporal power spectrum. In the present study, we tested directly the prediction that visual processing at the level of the LGN temporarily whitens the natural visual input. We recorded the responses of individual neurons in the LGN of the cat to natural, time-varying images (movies) and, as a control, to white-noise stimuli. Although there is substantial temporal correlation in natural inputs (Dong and Atick, 1995b), we found that the power spectra of LGN responses were essentially white. Between 3 and 15 Hz, the power of the responses had an average variation of only +/-10.3%. Thus, the signals that the LGN relays to visual cortex are temporarily decorrelated. Furthermore, the responses of X-cells to natural inputs can be well predicted from their responses to white-noise inputs. We therefore conclude that whitening of natural inputs can be explained largely by the linear filtering properties (Enroth-Cugell and Robson, 1966). Our results suggest that the early visual pathway is well adapted for efficient coding of information in the natural visual environment, in agreement with the prediction of the computational theory.

Hundreds of thalamic axons ramify within a column of cat visual cortex; yet each layer 4 neuron receives input from only a fraction of them. We have examined the specificity of these connections by recording simultaneously from layer 4 simple cells and cells in the lateral geniculate nucleus with spatially overlapping receptive fields (n ϭ 221 cell pairs). Because of the precise retinotopic organization of visual cortex, the geniculate axons and simple-cell dendrites of these cell pairs should have overlapped within layer 4. Nevertheless, monosynaptic connections were identified in only 33% of all cases, as estimated by cross-correlation analysis. The visual responses of monosynaptically connected geniculate cells and simple cells were closely related. The probability of connection was greatest when a geniculate center overlapped a strong simple-cell subregion of the same sign (ON or OFF) near the center of the subregion. This probability was further increased when the time courses of the visual responses were similar. In addition, the connections were strongest when the simple-cell subregion and the geniculate center were matched in position, sign, and size. The rules of connectivity between geniculate afferents and simple cells resemble those found for retinal afferents to geniculate cells. The connections along the retinogeniculocortical pathway, therefore, show a precision that goes beyond simple retinotopy to include many other response properties, such as receptive-field sign, timing, subregion strength, and size. This specificity in wiring emphasizes the need for developmental mechanisms (presumably correlation-based) that can select among afferents that differ only slightly in their response properties. Key words: visual cortex; simple cell; thalamus; thalamocortical; LGN; correlated firingAlthough separated by a single synapse, geniculate cells and cortical simple cells have very different response properties. Geniculate cells have receptive fields with a circular center and a concentric, antagonistic surround. Simple cells have receptive fields with elongated, parallel subregions. According to the original hypothesis of Hubel and Wiesel (1962), simple receptive fields are constructed from the convergence of geniculate inputs with receptive fields aligned in visual space. This hypothesis has received experimental support for simple cells in layer 4 of cat visual cortex Alonso, 1995, 1996;Ferster et al., 1996;Chung and Ferster, 1998). Specifically, if the receptive-field center of a geniculate cell overlaps a simple-cell subregion of the same sign (ON or OFF), then there is a high probability that the simple cell and the geniculate cell will be connected. Otherwise, the probability of finding a connection is almost zero (Reid and Alonso, 1995).The position and sign of receptive fields, however, may not be the only relevant factors in determining connectivity. Differences in response timing (Cleland et al., 1971a;Hoffmann et al., 1972; Mastronarde, 1987a,b;Humphrey and Weller, 1988;Wolfe and Palmer, 199...

In the visual cortex of higher mammals, neurons are arranged across the cortical surface in an orderly map of preferred stimulus orientations. This map contains 'orientation pinwheels', structures that are arranged like the spokes of a wheel such that orientation changes continuously around a centre. Conventional optical imaging first demonstrated these pinwheels, but the technique lacked the spatial resolution to determine the response properties and arrangement of cells near pinwheel centres. Electrophysiological recordings later demonstrated sharply selective neurons near pinwheel centres, but it remained unclear whether they were arranged randomly or in an orderly fashion. Here we use two-photon calcium imaging in vivo to determine the microstructure of pinwheel centres in cat visual cortex with single-cell resolution. We find that pinwheel centres are highly ordered: neurons selective to different orientations are clearly segregated even in the very centre. Thus, pinwheel centres truly represent singularities in the cortical map. This highly ordered arrangement at the level of single cells suggests great precision in the development of cortical circuits underlying orientation selectivity.