Response Facilitation From the “Suppressive” Receptive Field Surround of Macaque V1 Neurons

Abstract

Ichida JM, Schwabe L, Bressloff PC, Angelucci A. Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. J Neurophysiol 98: 2168 -2181, 2007. First published August 8, 2007 doi:10.1152/jn.00298.2007. 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 giving rise to 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 regions of the surround. 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 isoorientation 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 was 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 and inhibition, induced by surround stimulation, determine whether facilitation or suppression occurs. In layer 4C, the main target of geniculocortical afferents, lacking long-range intracortical connections, far-surround facilitation was rare and large surround fields were absent. This strongly suggests that feedforward connections do not contribute to far-surround modulation and that the latter is generated by intra-cortical mechanisms, likely involving top-down feedback.

Phase sensitivities, excitatory summation fields, and silent suppressive receptive fields of single neurons in the parastriate cortex of the cat

“…18 (present study) as well as in the case of cat area 17 (Sadakane et al 2006;Sengpiel et al 1997Sengpiel et al , 1998Song and Li 2008;Tailby et al 2007;Wang et al 2009) and areas V1 (Cavanaugh et al 2002;Ichida et al 2007;Kapadia et al 1999;Sceniak et al 1999;Sceniak et al 2001;Shushruth et al 2009) and V2 (Shushruth et al 2009) of macaque monkeys, the low-contrast-induced increases in the sizes of sRF were usually accompanied by significant decreases in the strength of suppressive surrounds. It has been argued that the low-contrast increases in the size of sRFs of cells in the primary visual cortices might be partially attributable to the accompanying strengthening of coupling of excitatory corticocortical synapses (Sceniak et al 1999) and/or inherited from the contrastdependent size tuning of the LGNd neurons (cf.…”

Towards Model-Based Brain Imaging with Multi-Scale Modeling

“…Interestingly, we also predicted that stimuli with a large separation from the receptive field of the recorded neuron could even facilitate (and not only suppress) the responses when the classical receptive field is stimulated at low contrast. Later we confirmed this prediction experimentally (Ichida et al, 2007). These studies show that stimulus-driven responses and their modulation can depend on the stimulus properties and are mediated by inter-areal connections.…”

“…In our modeling of visual cortical networks we also employed mean-field firing rate models as in NMMs (as well as more detailed models with so-called "spiking neurons"). We could show that single neuron responses in primary visual cortex (V1) are best explained when the local cortical microcircuits are assumed to operate in a balance between strong recurrent excitation and inhibition (Mariño et al, 2005a;Stimberg et al, 2009), and that inter-areal feedback into V1 may play a crucial role in "lateral inhibition" (Schwabe et al, 2006a;Ichida et al, 2007;Schwabe et al, 2010). To the best of our knowledge, such and other recent advances in cortical microcircuits models have not yet been implemented into NMMs used in brain imaging.…”

Stimulus Predictability Reduces Responses in Primary Visual Cortex

“…According to the model of Rao and Ballard (1999), this would require feedback from higher-level visual areas specifying which stimulus input is likely to arrive in V1 given the current spatiotemporal context. Feedback from higher-level visual areas to V1 seems a likely explanation for the effects of stimulus predictability reported here as these areas have larger receptive fields than V1, allowing them to determine the trajectory of long-range apparent motion (Angelucci and Bullier, 2003, Angelucci and Bressloff, 2006, Ichida et al, 2007. This fact, taken together with the observation that during long-range apparent motion hMT/V5ϩ sends feedback signals to V1 (Muckli et al, 2005;Sterzer et al, 2006;Ahmed et al, 2008;Wibral et al, 2008), can be considered a strong indication that activation in hMT/ V5ϩ drives the predictability effect in V1.…”