Although several lines of evidence suggest that stimulus selectivity in somatosensory and visual cortices is critically dependent on unselective inhibition, particularly in the thalamorecipient layer 4, no comprehensive comparison of the responses of excitatory and inhibitory cells has been conducted. Here, we recorded intracellularly from a large population of regular spiking (RS; presumed excitatory) and fast spiking (FS; presumed inhibitory) cells in layers 2-6 of primary visual cortex. In layer 4, where selectivity for orientation and spatial frequency first emerges, we found no untuned FS cells. Instead, the tuning of the spike output of layer 4 FS cells was significantly but moderately broader than that of RS cells. However, the tuning of the underlying synaptic responses was not different, indicating that the difference in spike-output selectivity resulted from differences in the transformation of synaptic input into firing rate. Layer 4 FS cells exhibited significantly lower input resistance and faster time constants than layer 4 RS cells, leading to larger and faster membrane potential (V(m)) fluctuations. FS cell V(m) fluctuations were more broadly tuned than those of RS cells and matched spike-output tuning, suggesting that the broader spike tuning of these cells was driven by visually evoked synaptic noise. These differences were not observed outside of layer 4. Thus, cell type-specific differences in stimulus feature selectivity at the first level of cortical sensory processing may arise as a result of distinct biophysical properties that determine the dynamics of synaptic integration.

To determine the locus, full extent, and topographic organization of cortical connections of area V4 (visual area 4), we injected anterograde and retrograde tracers under electrophysiological guidance into 21 sites in 9 macaques. Injection sites included representations ranging from central to far peripheral eccentricities in the upper and lower fields. Our results indicated that all parts of V4 are connected with occipital areas V2 (visual area 2), V3 (visual area 3), and V3A (visual complex V3, part A), superior temporal areas V4t (V4 transition zone), MT (medial temporal area), and FST (fundus of the superior temporal sulcus [STS] area), inferior temporal areas TEO (cytoarchitectonic area TEO in posterior inferior temporal cortex) and TE (cytoarchitectonic area TE in anterior temporal cortex), and the frontal eye field (FEF). By contrast, mainly peripheral field representations of V4 are connected with occipitoparietal areas DP (dorsal prelunate area), VIP (ventral intraparietal area), LIP (lateral intraparietal area), PIP (posterior intraparietal area), parieto-occipital area, and MST (medial STS area), and parahippocampal area TF (cytoarchitectonic area TF on the parahippocampal gyrus). Based on the distribution of labeled cells and terminals, projections from V4 to V2 and V3 are feedback, those to V3A, V4t, MT, DP, VIP, PIP, and FEF are the intermediate type, and those to FST, MST, LIP, TEO, TE, and TF are feedforward. Peripheral field projections from V4 to parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention. By contrast, the predominance of central field projections from V4 to inferior temporal areas is consistent with the need for detailed form analysis for object vision.

Excitatory lateral connections within the primary visual cortex are thought to link neurons with similar receptive field properties. Here we studied whether this rule can predict the distribution of excitatory connections in relation to cortical location and orientation preference in the cat visual cortex. To this end, we obtained orientation maps of areas 17 or 18 using optical imaging and injected anatomical tracers into these regions. The distribution of labeled axonal boutons originating from large populations of excitatory neurons was then analyzed and compared with that of individual pyramidal or spiny stellate cells. We demonstrate that the connection patterns of populations of nearby neurons can be reasonably predicted by Gaussian and von Mises distributions as a function of cortical location and orientation, respectively. The connections were best described by superposition of two components: a spatially extended, orientation-specific and a local, orientation-invariant component. We then fitted the same model to the connections of single cells. The composite pattern of nine excitatory neurons (obtained from seven different animals) was consistent with the assumptions of the model. However, model fits to single cell axonal connections were often poorer and their estimated spatial and orientation tuning functions were highly variable. We conclude that the intrinsic excitatory network is biased to similar cortical locations and orientations but it is composed of neurons showing significant deviations from the population connectivity rule.

Vision often requires attending to, and integrating information from, distant parts of the visual field. However, the neural basis for such long-range integration is not clearly understood. Here, we demonstrate a specific neural signature of attentional integration between stimuli in different parts of the visual field. Using functional MRI, we found that a task requiring the integration of information between two attended but spatially separated stimuli actively modulated the degree of functional integration (in terms of effective connectivity) between their retinotopic representations in visual cortical areas V1, V2, and V4. Spatial attention enhanced long-distance coupling between distinct neuronal populations that represented the attended visual stimuli, even at the earliest stages of cortical processing. In contrast, unattended stimulus representations were decoupled both from attended representations and particularly strongly from each other. Furthermore, enhanced functional integration between cortical representations was associated with enhanced behavioral performance. Attention may thus serve to "bind" together cortical loci at multiple levels of the visual hierarchy that are commonly involved in processing attended stimuli, promoting integration between otherwise functionally isolated cortical loci.