Suppressive waves disambiguate the representation of long-range apparent motion in awake monkey V1

The “apparent motion” illusion is evoked when stationary stimuli are successively flashed in spatially separated positions. It depends on the precise spatial and temporal separations of the stimuli. For large spatiotemporal separation, the long-range apparent motion (lrAM), it remains unclear how the visual system computes unambiguous motion signals. Here we investigated whether intracortical interactions within retinotopic maps could shape a global motion representation at the level of V1 population in response to a lrAM. In fixating monkeys, voltage-sensitive dye imaging revealed the emergence of a spatio-temporal representation of the motion trajectory at the scale of V1 population activity, shaped by systematic backward suppressive waves. We show that these waves are the expected emergent property of a recurrent gain control fed by the horizontal intra-cortical network. Such non-linearities explain away ambiguous correspondence problems of the stimulus along the motion path, preformating V1 population response for an optimal read-out by downstream areas. 2. peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/372763 doi: bioRxiv preprint first posted online Jul. 20, 2018; Chemla et al. Explaining away ambiguous representations in V1 When two stationary stimuli are successively flashed in spatially separated positions, it generates the so-called “apparent motion” illusion ​ . This illusion, well characterized in psychophysics ​ , depends on the spatio-temporal characteristics of the stimulus, being called “short-range” vs “long-range” apparent motion (lrAM) for spatial separation below or above 0.25° and temporal separation below or above 80 ms respectively ​ . In psychophysics, intrinsic differences were reported between these two types of apparent motion, however, there is some debate whether it is underlined by same or different process ​ . In physiology, while we have a clear idea on the neuronal processing generating direction-selective neuronal response to short-range apparent motion stimuli ​ , we still have a poor understanding of how the visual system process lrAM. This is probably because the spatial separation between individual strokes of the lrAM extend beyond the typical extent of receptive fields in the early visual system, at least in primates. In the case of the lrAM, psychophysicists have long highlighted the necessity to have a process, such as the “reviewing process” ​ , that will link the transient apparitions of stimuli in different spatial and temporal positions in order to generate a coherent motion percept of a single object, hereby solving the problem of “phenomenal identity” ​ 7​ or “correspondence” ​ . Downstream areas with large receptive fields are a natural expected integration unit for such extended spatiotemporal input. Indeed, it has been recently shown in human that the feedback from MT to V1 plays an important role in the processing of lrAM ​ , as well as evidences of downstream activation along the ventral stream ​ . However, it is still unclear whether and how the “reviewing” process, needed to keep track of the object identity along the motion trajectory, can be achieved within these receptive fields. As suggested from fMRI experiments in human, the neuronal processing within V1 could participate in formatting the representation of lrAM ​ . The extended precise retinotopic map in V1 makes it indeed an ideal platform for representing and disambiguating, at the level of the neuronal population, the trajectory of the apparent motion illusion, a representation that could be read-out by 3. peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/372763 doi: bioRxiv preprint first posted online Jul. 20, 2018; Chemla et al. Explaining away ambiguous representations in V1 downstream areas ​. In particular, V1 has the highest resolution ​ 15​ to achieve the interactions in space and time needed to link the individual strokes of the apparent motion ​ . In such context, intra-cortical and inter-cortical connectivity would be the natural substrate to underlie the necessary spatio-temporal interactions ​ . Importantly, these two networks have intrinsically different spatio-temporal properties, the inter-cortical network operating over very large extent but with poor spatial and temporal resolution , and the intra-cortical network has a more limited extent but with high spatial and temporal resolution ​ . Furthermore, they constitute the vast majority of synaptic contacts in the cortex, the feedback accounting for less than 20% and the intra-cortical connectivity contributing to 80% of the number of neuronal contacts, while the feedforward less than 1% ​ . Such connectivity seems therefore like a good candidate to link transient spatio-temporal events ​ . It was indeed shown, in the anesthetized cat, to shape visual information for a dynamic representations of sequences of static stimuli ​ 25,26​ through non-linear gain controls of the feedforward input ​ . However, it is still unclear whether and how the cortico-cortical interactions could participate to shape the representation of lrAM within V1 retinotopic map in the awake monkey. To answer this question, we used optical imaging of voltage-sensitive dyes (VSDI) in the awake fixating monkey, to measure how V1 neuronal population integrates a two-stroke lrAM that overreached individual neuronal receptive field size. In response to a single stroke, activity in V1 propagates in space and time, as already documented ​ , with spatial and temporal constants that cover about 3 mm and 80 ms. In response to the lrAM of various spatio-temporal separations, we observed that the cortical response systematically deviates from the linear prediction and generates a wave of suppression that is initiated right at the second stimulus onset and propagates to suppress the residual response to the first stimulus. A computational model was developed to understand the potential origin of such suppressive waves. The model shows that two ingredients are necessary to explain suppressive waves: the higher gain of inhibitory cells, and the shunting effect of the associated 4. peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which was not . http://dx.doi. org/10.1101/372763 doi: bioRxiv preprint first posted online Jul. 20, 2018; Chemla et al. Explaining away ambiguous representations in V1 synaptic conductances. Using a spatio-temporal decoding approach, we demonstrate that such suppression waves explain away ambiguous representation of stimulus position along the apparent motion trajectory. We suggest that these waves preformat V1 population response for an unambiguous representation of the lrAM that could be optimally read-out by downstream areas.