Abstract
Previous studies indicate that top-down influence plays a critical role in visual information processing and perceptual detection. However, the substrate that carries top-down influence remains poorly understood. Using a combined technique of retrograde neuronal tracing and immunofluorescent double labeling, we characterized the distribution and cell type of feedback neurons in cat’s high-level visual cortical areas that send direct connections to the primary visual cortex (V1: area 17). Our results showed: (1) the high-level visual cortex of area 21a at the ventral stream and PMLS area at the dorsal stream have a similar proportion of feedback neurons back projecting to the V1 area, (2) the distribution of feedback neurons in the higher-order visual area 21a and PMLS was significantly denser than in the intermediate visual cortex of area 19 and 18, (3) feedback neurons in all observed high-level visual cortex were found in layer II–III, IV, V, and VI, with a higher proportion in layer II–III, V, and VI than in layer IV, and (4) most feedback neurons were CaMKII-positive excitatory neurons, and few of them were identified as inhibitory GABAergic neurons. These results may argue against the segregation of ventral and dorsal streams during visual information processing, and support “reverse hierarchy theory” or interactive model proposing that recurrent connections between V1 and higher-order visual areas constitute the functional circuits that mediate visual perception. Also, the corticocortical feedback neurons from high-level visual cortical areas to the V1 area are mostly excitatory in nature.
Highlights
It is widely assumed for a long time that visual perception is formed step by step in a feedforward mode from the retina to LGN, to the primary visual cortex (V1), and to higher-order visual cortical areas (Hubel and Wiesel, 1968; Hirsch, 2003; Herzog and Clarke, 2014)
Two-way ANOVA indicated that the proportion of CaMKII/Retrobeads double-positive neuron (CRN) neurons to NRNs showed a significant variation among different high-level visual cortical areas (main effect of the area: F(3,464) = 93.38, p < 0.0001), and between different cortical layers (effect of layer: F(3,464) = 6.096, p < 0.0001; Figure 7); there was a significant interaction between cortical areas and cortical layers (interaction of area × layer: F(9,464) = 1.96, p = 0.042)
It is traditionally assumed that visual information is processed in a feedforward hierarchical model that simple visual features are coded at the primary (V1) or low-level visual cortex, and complex visual attributes converged at higher-order visual areas for perceptual output (Juan and Walsh, 2003; Ro et al, 2003; Briggs and Usrey, 2011; Klink et al, 2017)
Summary
It is widely assumed for a long time that visual perception is formed step by step in a feedforward mode from the retina to LGN, to the primary visual cortex (V1), and to higher-order visual cortical areas (Hubel and Wiesel, 1968; Hirsch, 2003; Herzog and Clarke, 2014). The visual system of a cat may have a ventral-dorsal information processing manner similar to that of primate (Dreher et al, 1996b; Wang et al, 2007; Tong et al, 2011), but supporting evidence is quite limited so far (Connolly et al, 2012). Some authors have taken efforts to define the feedback projections using retrograde and anterograde tracing techniques (Olson and Lawler, 1987; Dreher et al, 1996a; Fitzgibbon et al, 1999; Han et al, 2008; Connolly et al, 2012; Yang X. et al, 2016), information about the distribution and cell types of feedback neurons in different high-level cortical areas are quite limited. Using a combined technique of retrograde neuronal tracing and immunofluorescent double labeling, this study compared the proportion and cell type of neurons in cat’s different higherlevel visual cortical areas that send direct feedback projections to the V1 area, trying to expand our understanding of the characteristics and mechanisms of top-down influence
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