The role of feedback projections in feature tuning and neuronal excitability in the early primate visual system.

A general assumption in visual neuroscience is that basic receptive field properties such as orientation and direction selectivity are constructed within intrinsic neuronal circuits and feedforward projections. In addition, it is assumed that general neuronal excitability and responsiveness in early visual areas is to a great extent independent of feedback input originating in areas higher in the stream. Here, we review the contribution of feedback projections from MT, V4 and pulvinar to the receptive field properties of V2 neurons in the anesthetized and paralyzed monkey. Importantly, our results contradict both of these assumptions. We separately inactivated each of these three brain regions using GABA pressure injections, while simultaneously recording V2 single unit activity before and hours after inactivation. Recordings and GABA injections were carried out in topographically corresponding regions of the visual field. We outline the changes in V2 activity, responsiveness and receptive field properties for early, mid and late post-injection phases. Immediately after injection, V2 activity is globally suppressed. Subsequently, there is an increase in stimulus-driven relative to spontaneous neuronal activity, which improves the signal-to-noise coding for the oriented moving bars. Notably, V2 tuning properties change substantially relative to its pre-injection selectivity profile. The resulting increase or decrease in selectivity could not be readily predicted based on the selectivity profile of the inactivated site. Finally, V2 activity rebounds before returning to it pre-injection profile Our results show that feedback projections profoundly impact neuronal circuits in early visual areas, and may have been heretofore largely underestimated in their physiological role.

Effects of inactivation of the lateral pulvinar on response properties of second visual area cells in Cebus monkeys.

1. In the present study, we investigated the influence of the pulvinar nucleus upon response properties of single cells in the second visual area (V2) of Cebus monkeys. The method used consisted of the inactivation of a portion of the lateral pulvinar by GABA injections while studying the response properties of cells in V2 at the same visuotopic location as that of the inactivation. 2. After GABA injection in the pulvinar, most cells in V2 (67%) showed changes in spontaneous and/or stimulus-driven activities. Contrary to the effect found with inactivation of the striate cortex, which promotes a reduction in the response of V2 neurons, we found that the main effect of pulvinar inactivation was an increment in stimulus-driven responses of V2 cells (39% of units studied). A reduction of responses was observed in 27% of units. 3. A change in orientation and/or direction selectivity was found in 91% of cells after inactivation of the pulvinar. Most commonly, the orientation selectivity of a neuron was decreased during pulvinar inactivation. 4. The inactivation results indicate that the pulvinar projections have a modulatory effect on the activity of V2 cells.

Distribution of NADPH-diaphorase in the superior colliculus of Cebus monkeys, and co-localization with calcium-binding proteins.

We examined the distribution of the enzyme dihydronicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) in the superior colliculus (SC) of the New World monkey Cebus apella, and the co-localization of this enzyme with the calcium-binding proteins (CaBPs) calbindin-D28K, parvalbumin and calretinin. Despite the intensely labeled neuropil, rare NADPH-d-positive cells were observed in the stratum griseum superficiale (SGS). Most of the labeled cells in the SC were found in the intermediate layers, with a great number also in the deeper layers. This pattern is very similar to that described in the opossum (Didelphis marsupialis) and in the cat, and different from the pattern found in the rat, which shows labeled cells mainly in the SGS. Cells doubly stained for NADPH-d and CaBPs were observed throughout the SC, although in a small number. Of the NADPH-d-positive cells, 20.3% were doubly labeled for NADPH-d and parvalbumin, 10.2% revealed co-localization with calretinin, and 5.6% with calbindin. The low number of double-stained cells for NADPH-d and the CaBPs indicates that these molecules must participate in different functional circuits within the SC.