We investigated the spatiotemporal activation pattern, produced by one visual stimulus, across cerebral cortical regions in awake monkeys. Laminar profiles of postsynaptic potentials and action potentials were indexed with current source density (CSD) and multiunit activity profiles respectively. Locally, we found contrasting activation profiles in dorsal and ventral stream areas. The former, like V1 and V2, exhibit a 'feedforward' profile, with excitation beginning at the depth of Lamina 4, followed by activation of the extragranular laminae. The latter often displayed a multilaminar/columnar profile, with initial responses distributed across the laminae and reflecting modulation rather than excitation; CSD components were accompanied by either no changes or by suppression of action potentials. System-wide, response latencies indicated a large dorsal/ventral stream latency advantage, which generalizes across a wide range of methods. This predicts a specific temporal ordering of dorsal and ventral stream components of visual analysis, as well as specific patterns of dorsal-ventral stream interaction. Our findings support a hierarchical model of cortical organization that combines serial and parallel elements. Critical in such a model is the recognition that processing within a location typically entails multiple temporal components or 'waves' of activity, driven by input conveyed over heterogeneous pathways from the retina.
We measured the timing, areal distribution, and laminar profile of fast, wavelength-insensitive and slower, wavelength-sensitive responses in V1 and extrastriate areas, using laminar current-source density analysis in awake macaque monkeys. There were 3 main findings. 1) We confirmed previously reported significant ventral-dorsal stream latency lags at the level of V4 (V4 mean = 38.7 ms vs. middle temporal mean = 26.9 ms) and inferotemporal cortex (IT mean = 43.4 ms vs. dorsal bank of the superior temporal sulcus mean = 33.9 ms). 2) We found that wavelength-sensitive inputs in areas V1, V4, and IT lagged the wavelength-insensitive responses by significant margins; this lag increased over successive levels of the system. 3) We found that laminar activation profiles in V4 and IT were inconsistent with "feedforward" input through the ascending ventral cortical pathway; the likely alternative input routes include both lateral inputs from the dorsal stream and direct inputs from nonspecific thalamic neurons. These findings support a "Framing" Model of ventral stream visual processing in which rapidly conducted inputs, mediated by one or more accessory pathways, modulate the processing of more slowly conducted feedforward inputs.
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