Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey

Abstract

The nonretinotopic portion of the macaque pulvinar complex is interconnected with the occipitoparietal and occipitotemporal transcortical visual systems where information about the location and motion of a visual object or its form and color are modulated by eye movements and attention. We recorded from single cells in and about the border of the dorsal portion of the lateral pulvinar and the adjacent medial pulvinar of awake behaving Macaca mulatto in order to determine how the properties of these two functionally dichotomous cortical systems were represented. We found a class of pulvinar neurons that responded differentially to ten different patterns or broadband wavelengths (colors). Thirty-four percent of cells tested responded to the presentation of at least one of the pattern or color stimuli. These cells often discharged to several of the patterns or colors, but responded best to only one or two of them, and 86% were found to have statistically significant pattern and/or color preferences. Pattern/color preferential cells had an average latency of 79.1 ± 46.0 ms (range 31-186 ms), responding well before most inferotemporal cortical cell responses. Visually guided and memory-guided saccade tasks showed that 58% of pattern/color preferential cells also had saccade-related properties, e.g. directional presaccadic and postsaccadic discharges, and inhibition of activity during the saccade. In the pulvinar, the mean presaccadic response latency was earlier, and the mean postsaccadic response latency was later, than those reported for parietal cortex. We also discovered that the strength of response to patterns or colors changed depending upon the behavioral setting. In comparison to trials in which the monkey fixated dead ahead during passive presentations of pattern and color stimuli, 92% of the cells showed attenuated responses to the same passive presentation of patterns and colors during fixation when these trials were interleaved with trials which also required active saccades to pattern and color targets in the periphery. We conclude that properties which represent the functionally dichotomous object and spatial visual systems are found together in single pulvinar neurons and that the responses of these cells to pattern or color stimuli are influenced by the focus of spatial attention. The pulvinar is the first structure in the brain shown to have neurons which integrate both object and spatial properties and the response latencies indicate that this information is processed before that in cortex. These results are discussed in terms of role of the pulvinar in visual attention as well as its unique role in providing both object feature and spatial location information to the inferotemporal cortex.

The Anatomical and Functional Organization of the Human Visual Pulvinar

“…The dorsal medial pulvinar did not show clear contralateral tuning and was mainly interconnected with parietal and frontal cortex in humans. This is comparable with the organization of the dorsal medial pulvinar in other primates (Yeterian and Pandya, 1985;Schmahmann and Pandya, 1990;Benevento and Port, 1995;Gutierrez et al, 2000;Wilke et al, 2010).…”

Perceptual Switching, Eye Movements, and the Bus Paradox

“…The combination of increased activity in higher-order visual areas and reduced activity in the primary visual cortex and the pulvinar (Kleinschmidt et al 1998) could be understood as the result of top^down mediated initiation of the switch, together with sensory suppression. Suppressed activity in the primary visual cortical areas as well as in the pulvinar are known to occur during saccades (Benevento and Port 1995), and their occurrence in perceptual switching may well be the result of enhanced saccade frequency. In this respect, saccades and blinks have the same effect.…”

“…The pulvinar belongs to the secondary visual system known to be involved in calibrating the visual image with respect to movement of the eyes. Whereas there is enhanced activity before and after the saccade, reduced activity in the pulvinar has been observed in monkey during saccades (Benevento and Port 1995). Saccades are known also to lead to sensory suppression (Volkmann et al 1980;Uchikawa and Sato 1995;Ridder and Tomlinson 1997), leading in turn to reduced activity in the early visual cortical areas.…”

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

“…The medial and lateral pulvinar have been suggested to assist in shifting attention to relevant visual stimuli (15)(16)(17). Biologically meaningful stimuli relevant to our primate ancestors must have included snakes (1, 2, 5).…”