Distinct Feedforward and Feedback Effects of Microstimulation in Visual Cortex Reveal Neural Mechanisms of Texture Segregation

Abstract

The visual cortex is hierarchically organized, with low-level areas coding for simple features and higher areas for complex ones. Feedforward and feedback connections propagate information between areas in opposite directions, but their functional roles are only partially understood. We used electrical microstimulation to perturb the propagation of neuronal activity between areas V1 and V4 in monkeys performing a texture-segregation task. In both areas, microstimulation locally caused a brief phase of excitation, followed by inhibition. Both these effects propagated faithfully in the feedforward direction from V1 to V4. Stimulation of V4, however, caused little V1 excitation, but it did yield a delayed suppression during the late phase of visually driven activity. This suppression was pronounced for the V1 figure representation and weaker for background representations. Our results reveal functional differences between feedforward and feedback processing in texture segregation and suggest a specific modulating role for feedback connections in perceptual organization.

Stimulus content shapes cortical response statistics

“…It has been shown that variance in mean responses in V2 can be well predicted by variations in factors that determine the statistics necessary for the generation of natural textures, while variations in mean responses in V1 can be predicted by variations in statistics at the level of independent Gabor-like edge filters. Similarly, contextual modulation of V1 activity by top-down influences from V2 neurons was demonstrated when high-level inferences were made in artificial images (Klink et al, 2017;Lee and Nguyen, 2001). These results can be explained in terms of probabilistic inference in a hierarchical internal model of natural images, in which mean responses correspond to the most probable interpretation of the stimulus.…”

“…Investigations into the organization of feedback revealed that characteristic regularities present in the visual environment are reflected in the structure of both lateral (Kaschube, 2014;Löwel and Singer, 1992;McGuire et al, 1991;Schmidt et al, 1997;G. B. Smith et al, 2015) and top-down (Klink et al, 2017;Lee and Nguyen, 2001) interactions. These feedback interactions could thus establish dependencies between the responses of neurons whose receptive fields are sensitive to stimulus features that have high probability to co-occur in the visual environment and support perceptual grouping, such as the vicinity, continuity, collinearity, color and direction of motion of composing scene elements.…”

“…Indeed, on a pebbly beach we expect different cooccurrence patterns of elementary edges, characteristic to V1 simple cell receptive fields, than on a wheat field. Furthermore, given that the visual cortex processes visual information in a series of hierarchical processing stages, contextual information from the higher levels of the processing hierarchy can inform and constrain the activity at lower levels of processing through feedback (Gilbert and Sigman, 2007;Klink et al, 2017;Lee and Mumford, 2003). For instance, merging information from an extended area in the visual field will inform low-level stages of the processing hierarchy that we are on a beach and the expected textures are characterized by specific spatial frequencies and lines are characterized by specific curvatures.…”

Cortical travelling waves: mechanisms and computational principles

“…As outlined above, while most studies have focused on waves during the stimulus onset response, travelling waves may be induced during sustained stimulation responses and during the brief increase of spiking activity at stimulus offset in the sensory cortex of awake, behaving animals, and these waves may not be time-locked to the stimulus. Bursts during the fast onset transient arise through feedforward input; however, during spontaneous and induced waves, these bursts can result from recurrent fluctuations or feedback connections 26,106 . Nevertheless, initial evidence indicates that induced waves travel over similar fibre networks as waves evoked during stimulus onset 66,77 .…”

Cortical Hierarchy, Dual Counterstream Architecture and The Importance of Top-Down Generative Networks

“…In contrast to FF-pathways, the neurobiology of the significantly more numerous FB pathways (Markov et al, 2014a) An early conceptualization of hierarchical processing in the cortex conceived of FF pathways driving target areas, and in contrast FB pathways merely exerting a modulatory influence (Klink et al, 2017), however, some researchers hold a more nuanced view (Bastos et al, 2012). Indeed, the simple dichotomy of the roles of FF and FB pathways is difficult to reconcile with the multiple physiological effects that are imputed to FB control.…”