Hæmodynamic signals underlying functional brain imaging (e.g. fMRI) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in hæmodynamic signal implying equal increases in the underlying neuronal activity1-6. Few studies have compared neuronal and hæmodynamic signals in alert animals7,8 to test for this assumed correspondence. Here we present evidence bringing this assumption into question. Using a dual-wavelength optical imaging technique9 that independently measures cerebral blood volume and oxygenation, continuously, in alert behaving monkeys, we find two distinct components to the hæmodynamic signal in the alert animals' primary visual cortex (V1). One component is reliably predictable from neuronal responses generated by visual input. The other component – of almost comparable strength – is a hitherto unknown signal that entrains to task structure independent of visual input or of standard neural predictors of hæmodynamics. This latter component shows predictive timing, with increases of cerebral blood volume in anticipation of trial onsets even in darkness. This trial-locked hæmodynamic signal could be due to an accompanying V1 arterial pumping mechanism, closely matched in time, with peaks of arterial dilation entrained to predicted trial onsets. These findings (tested in 2 animals) challenge the current understanding of the link between brain hæmodynamics and local neuronal activity. They also suggest the existence of a novel preparatory mechanism in the brain that brings additional arterial blood to cortex in anticipation of expected tasks.

Two components of cortical circuits could mediate contour integration in primary visual cortex (V1): intrinsic horizontal connections and feedback from higher cortical areas. To distinguish between these, we combined functional mapping with a new technique for labeling axons, a recombinant adenovirus bearing the gene for green fluorescent protein (GFP), to determine the extent, density, and orientation specificity of V1 intrinsic connections and V2 to V1 feedback. Both connections cover portions of V1 representing regions of visual space up to eight times larger than receptive fields as classically defined, though the intrinsic connections are an order of magnitude denser than the feedback. Whereas the intrinsic connections link similarly oriented domains in V1, V2 to V1 feedback displays no such specificity. These findings suggest that V1 intrinsic horizontal connections provide a more likely substrate for contour integration.

The cortical 'point spread' (PS) is the area of cortex activated by a minimal visual stimulus. Here we use the PS to explore the functional role of lateral connectivity in normal cat primary visual cortex (V1) and its involvement in topographic reorganization of cortex following retinal lesions. We compared the distributions of PSs measured with optical recording, which reflects both spiking and subthreshold activity, with those measured with extracellular electrodes, which reveal spiking activity alone. The spiking PS represented only 5% of the area of activation shown in the optical PS, indicating that the remaining 95% was probably generated by subthreshold activation. The orientation dependence of the pattern of the subthreshold activation and its close match with orientation columns suggests that long-range horizontal connections radiating from the locus of spiking activity were responsible for the observed activation. The spike PS showed anisotropies and inhomogeneities that were related to the pattern of orientation columns and indicated distortions in the representation of visual space on the cortical surface. In the reorganized cortex the spike PS expanded, approximating the extent of the optical PS seen in normal cortex, and suggesting that reorganization was mediated by an unmasking of normally subthreshold activation to suprathreshold levels. The orientation map of the reorganized cortex showed a close match to that obtained before placing the lesion, despite the large shift in topography, supporting the idea that intrinsic horizontal connections were responsible for the remapping.

Neurons in primary visual cortex (V1) respond differently to a simple visual element presented in isolation from when it is embedded within a complex image. This difference, a specific modulation by surrounding elements in the image, is mediated by short- and long-range connections within V1 and by feedback from other areas. Here we study the role of short-range connections in this process, and relate it to the layout of local inhomogeneities in the cortical maps of orientation and space. By measuring correlation between neuron pairs located in optically imaged maps of V1 orientation columns we show that the strength of local connections between cells is a graded function of lateral separation across cortex, largely radially symmetrical and relatively independent of orientation preferences. We then show the contextual influence of flanking visual elements on neuronal responses varies systematically with a neuron's position within the cortical orientation map. The strength of this contextual influence on a neuron can be predicted from a model of local connections based on simple overlap with particular features of the orientation map. This indicates that local intracortical circuitry could endow neurons with a graded specialization for processing angular visual features such as corners and T junctions, and this specialization could have its own functional cortical map, linked with the orientation map.

Cells in adult primary visual cortex are capable of integrating information over much larger portions of the visual field than was originally thought. Moreover, their receptive field properties can be altered by the context within which local features are presented and by changes in visual experience. The substrate for both spatial integration and cortical plasticity is likely to be found in a plexus of long-range horizontal connections, formed by cortical pyramidal cells, which link cells within each cortical area over distances of 6-8 mm. The relationship between horizontal connections and cortical functional architecture suggests a role in visual segmentation and spatial integration. The distribution of lateral interactions within striate cortex was visualized with optical recording, and their functional consequences were explored by using comparable stimuli in human psychophysical experiments and in recordings from alert monkeys. They may represent the substrate for perceptual phenomena such as illusory contours, surface fill-in, and contour saliency. The dynamic nature of receptive field properties and cortical architecture has been seen over time scales ranging from seconds to months. One can induce a remapping of the topography of visual cortex by making focal binocular retinal lesions. Shorter-term plasticity of cortical receptive fields was observed following brief periods of visual stimulation. The mechanisms involved entailed, for the short-term changes, altering the effectiveness of existing cortical connections, and for the long-term changes, sprouting of axon collaterals and synaptogenesis. The mutability of cortical function implies a continual process of calibration and normalization of the perception of visual attributes that is dependent on sensory experience throughout adulthood and might further represent the mechanism of perceptual learning.