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J Neurophysiol (August 8, 2007). doi:10.1152/jn.00298.2007
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Submitted on March 16, 2007
Accepted on August 8, 2007

Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons

Jennifer M. Ichida1, Lars Schwabe2, Paul C Bressloff3, and Alessandra Angelucci1*

1 Ophthalmology, Moran Eye Center, University of Utah, Salt Lake City, Utah, United States
2 Ophthalmology, Moran Eye Center, University of Utah, Salt Lake City, Utah, United States; Mathematics, University of Utah, Salt Lake City, Utah, United States
3 Mathematics, University of Utah, Salt Lake City, Utah, United States

* To whom correspondence should be addressed. E-mail: alessandra.angelucci{at}hsc.utah.edu.

In primary visual cortex (V1), neuronal responses to optimally-oriented stimuli in the receptive field (RF) center are usually suppressed by iso-oriented stimuli in the RF surround. The mechanisms and pathways underlying surround modulation, a possible neural correlate of perceptual figure-ground segregation, are not yet identified. We previously proposed that highly-divergent and fast-conducting top-down feedback connections are the substrate for fast modulation arising from the more distant surround regions. We have recently implemented this idea into a recurrent network model (Schwabe et al. 2006). The purpose of this study was to test a crucial prediction of this feedback model, namely that the suppressive "far surround of V1 neurons can be facilitatory under conditions that weakly activate neurons in the RF center. Using single unit recordings in macaque V1, we found iso-orientation far surround facilitation when the RF center was driven by a low-contrast stimulus, and the far surround by a small annular stimulus. Suppression occurred when the center stimulus contrast or the size of the surround stimulus were increased. This suggests that center-surround interactions result from excitatory and inhibitory mechanisms of similar spatial extent, and that changes in the balance of local excitation/inhibition, induced by surround stimulation, determine whether facilitation or suppression occurs. In layer 4C, the main target of geniculocortical afferents, lacking long-range intra-cortical connections, far surround facilitation was rare and large surround fields were absent. Thus, feedforward connections are unlikely to contribute to far surround modulation; the latter is instead generated by intra-cortical mechanisms, likely involving top-down feedback.




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