Eye Position Influence on the Parieto‐occipital Area PO (V6) of the Macaque Monkey

Abstract

The aim of this work was to study the effect of eye position on the activity of neurons of area PO (V6), a cortical region located in the most posterior part of the superior parietal lobule. Experiments were carried out on three awake macaque monkeys. Animals sat in a primate chair in front of a large screen, and fixated a small spot of light projected in different screen locations while the activity of single neurons was extracellularly recorded. Both visual and non-visual neurons were found. About 48% of visual and 32% of non-visual neurons showed eye position-related activity in total darkness, while in approximately 61% of visual response was modulated by eye position in the orbit. Eye position fields and/or gain fields were different from cell to cell, going from large and quite planar fields up to peak-shaped fields localized in more or less restricted regions of the animal's field of view. The spatial distribution of fixation point locations evoking peak activity in the eye position-sensitive population did not show any evident laterality effect, or significant top/bottom asymmetry. Moreover, the cortical distribution of eye position-sensitive neurons was quite uniform all over the cortical region studied, suggesting the absence of segregation for this property within area PO (V6). In the great majority of visual neurons, the receptive field 'moved' with gaze according to eye displacements, remaining at the same retinotopic coordinates, as is usual for visual neurons. In some cases, the receptive field did not move with gaze, remaining anchored to the same spatial location regardless of eye movements ('real-position cells'). A model is proposed suggesting how eye position-sensitive visual neurons might build up real-position cells in local networks within area PO (V6). The presence in area PO (V6) of real-position cells together with a high percentage of eye position-sensitive neurons, most of them visual in nature, suggests that this cortical area is engaged in the spatial encoding of extrapersonal visual space. Since lesions of the superior parietal lobule in humans produce deficits in visual localization of targets as well as in arm-reaching for them, and taking into account that the monkey's area PO (V6) is reported to be connected with the premotor area 6, we suggest that area PO (V6) supplies the premotor cortex with the visuo-spatial information required for the visual control of arm-reaching movements.

Implementation of Spatial Transformation Rules for Goal-Directed Reaching via Gain Modulation in Monkey Parietal and Premotor Cortex

“…Gain modulation of spatially selective neurons is the key principle underlying the spatial transformation mechanism in this model, similar to previous models of multisensory integration for spatial reference frame transformations (Zipser and Andersen, 1988;Salinas and Abbott, 1996). Gain modulation during multisensory integration for eye or hand movements had previously been found in the posterior parietal cortex (Andersen et al, 1985;Brotchie et al, 1995;Galletti et al, 1995;Snyder et al, 1998;Batista et al, 1999;Nakamura et al, 1999;Buneo et al, 2002) and frontal areas (Boussaoud et al, , 1998Mushiake et al, 1997;Cisek and Kalaska, 2002). In contrast, here we have shown gain modulation effects in PRR and PMd for remapping visuospatial information onto reach motor goals according to abstract cognitive transformation rules.…”

“…Based on our data, we propose that gain modulation is used by the brain not only in sensorimotor areas to achieve reference frame transformations driven by multisensory input (Andersen et al, 1985;Zipser and Andersen, 1988;Boussaoud et al, , 1998Brotchie et al, 1995;Galletti et al, 1995;Buneo et al, 2002), but also in the frontoparietal reach network to achieve contextually modulated, goal-directed visuomotor remapping, as previously suggested theoretically (Salinas, 2004;Brozovic´et al, 2007). Our current data support this idea by providing first experimental evidence for context-specific gain modulations of spatial motor-goal tuning in PRR and PMd, which could denote the key underlying principle of flexible goal-directed behavior.…”

“…Computational models suggest that this flexibility can be achieved with contextual gain modulation of spatially selective neurons (Salinas, 2004;Brozovic´et al, 2007), equivalent to gain field mechanisms suggested for multisensory integration (Andersen et al, 1985;Zipser and Andersen, 1988;Boussaoud et al, , 1998Brotchie et al, 1995;Galletti et al, 1995;Salinas and Abbott, 1996;Snyder et al, 1998;Salinas and Thier, 2000). If the idea of gain modulation for space-context integration holds true, then spatially selective neurons in primate cortical sensorimotor areas, like the parietal reach region (PRR) and the dorsal premotor cortex (PMd), should be upregulated and downregulated by the behavioral context.…”

Coinciding early activation of the human primary visual cortex and anteromedial cuneus

“…14 and 25) should have pushed the functional area V6 from the medial fundus of the parieto-occipital sulcus in monkeys (22) to the upper posterior wall of the parietooccipital sulcus and thus to the anteromedial cuneus in humans. The neurons of V6 have large receptive fields (22), and lack enhanced foveal magnification both in monkeys (22) and humans (26), and the area has been suggested to participate in visuospatial analysis of environment for arm reaching and eye movements (27,28). The human anteromedial cuneus could also contain an area or multiple areas with no equivalent in the macaque brain.…”

Eye Position Encoding in Three-Dimensional Space: Integration of Version and Vergence Signals in the Medial Posterior Parietal Cortex

“…Several neurophysiological studies have shown that the activity of neurons in many PPC areas is modulated by gaze direction (Sakata et al, 1980;Mountcastle, 1981;Andersen and Mountcastle, 1983;Andersen et al, 1990;Galletti et al, 1995;Squatrito and Maioli, 1996;Bremmer et al, 1997Bremmer et al, , 2001Nakamura et al, 1999), but few have demonstrated that single PPC neurons are modulated by vergence (Sakata et al, 1980;Genovesio and Ferraina, 2004;Genovesio et al, 2007;Bhattacharyya et al, 2009). The encoding of both direction of gaze and depth of fixation in single PPC neurons has been to date reported only in area 7a (Sakata et al, 1980).…”