Horizontal Connectivity and Prediction of Coherences in the Integration of Contour and Motion in the Primary Visual Cortex

"This talk explores the possibility that horizontal intra-cortical connections contribute to the dynamic emergence of facilitation and predictions in the primary visual cortex (V1) of cat and non-human primates (NHP)). Contextual long-range interactions, studied at the spiking level, are generally thought to depend on cortico-cortical feedback (Li et al., 2006; Gilbert and Li, 2013) and attention (Lamme & Roelfsema 2000). In contrast, the contribution of intra-V1 mechanisms such as recurrent amplification and lateral propagation (review in Frégnac, 2002 and Frégnac and Bathellier, 2015) is less known.

Experimental work in my lab (UNIC) has been focusing on the dynamic processes based on lateral propagation in V1, through which spatio-temporal inferences (continuous movement or apparent motion sequences) may be generated and facilitate predictive responses along a trajectory (""filling-in""). The stimulation paradigms that we have designed interleave a variety of apparent or continuous animations of local oriented stimuli along trajectories, forming predictable global patterns according to their local to global configuration, and their specific spatial and temporal properties. We have measured the cortical dynamics evoked at two scales of neuronal integration, from micro- (intracellular, SUA) to meso-scopic levels (dense laminar electrode (MEA) and voltage sensitive dye imaging (VSDI)) in the anesthetized cat.

The picture drawn from our intracellular observations is that synaptic activity in cat V1 reveals a built-in bias in the structural organization in the absence of attention-related feedback from higher cortical areas (Gerard-Mercier et al, 2016). This neural process could be related to perceptual biases expressed in NHPs and humans. Taken together with findings obtained in collaboration with the group of Frederic Chavane (INT, Marseille), and based on LFP recordings (Benvenuti et al, submitted), our results suggest, surprisingly, that distinct neural mechanisms - implicating horizontal connectivity - may operate along orthogonal configurations of orientation and direction features and activate differently V1 receptive fields (RF): on one side, surround facilitatory modulation along the orientation preference axis; on the other, anticipatory responses for direction perpendicular to orientation, i.e. along the RF width axis.

Each set of data (still in progress) points to two specific roles of horizontal propagation in V1, with possibly different spatial anisotropy profiles, different spatial scales and different speed selectivities. The first one concerns collinear-biased propagation of iso-orientation preference at high speed (0.1-0.3 m/s; 100°/sec (monkey) -250°/sec (cat)) and fits the general concept of the ""perceptual"" association field” (Field et al, 1993; Li et al, 2006; Gerard-Mercier et al, 2016). The second one concerns isotropic horizontal propagation (10-30°/sec (cat and monkey)) and the directional build-up of anticipatory activity facilitating integration of a moving object along a trajectory (Benevenuti et al, submitted). This propagation process could operate at lower speed than the orientation selective component, and most likely imply a cascade of shorter-range horizontal interactions triggered by a sequence of feedforward inputs. Its synaptic correlates are still unknown.

At a more conceptual level, our working hypothesis posits that horizontal connectivity participates to the propagation of a network-based belief, resulting in some kind of ""prediction"" (filling-in) or ""anticipatory"" build-up process travelling through the V1 network. This view may be compared - and why not opposed - to the classical ""predictive coding"" schema (Rao and Ballard, 1999) where what is transmitted laterally or through feedback onto V1 is the error signal itself (error from the expectation generated in higher cortical areas) rather than the prediction inferred from the global perceptual information. When the contrast is high, the lateral broadcast of the peripheral context leads to a suppression of redundancy of activity in V1 (Martin and von der Heydt, 2015). In contrast when the feedforward signal is weak (low contrast or stimulus absence in ""illusory contour"") the contextual information boosts the gain of feedforward-related activity (Fregnac et al, 1996). Future project development focuses on the possible dependency of the balance between horizontal connectivity and feedback from higher cortical areas on species-specific V1 architecture features and cognitive behavior.

This work, in its initial phase, has been supported by the ramp-up phase of the Human Brain Project (HBP-SP3), and the Marie-Curie Fellowship program. It is currently funded by the CNRS and the French Agence Nationale de la Recherche (ANR: Horizontal-V1).

References :

Benvenuti, G., Chemla, S., Boonman, A., Masson, GS and Chavane F (submitted). Anticipatory responses along motion trajectories in awake monkey V1.
Chavane, F., Sharon, D., Jancke, D., Marre, O., Frégnac, Y., & Grinvald, A. (2011). Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity. Frontiers in Systems Neuroscience, 5(4): 1-26.
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