Motion contrast in primary visual cortex: a direct comparison of single neuron and population encoding

Abstract

Features from outside the classical receptive field (CRF) can modulate the stimulus-driven activity of single cells in the primary visual cortex. This modulation, mediated by horizontal and feedback networks, has been extensively described as a variation of firing rate and is considered the basis of processing features as, for example, motion contrast. However, surround influences have also been identified in pairwise spiking or local field coherence. Yet, evidence about co-existence and integration of different neural signatures remains elusive. To compare multiple signatures, we recorded spiking and LFP activity evoked by stimuli exhibiting a motion contrast in the CRFs surround in anesthetized cat primary visual cortex. We chose natural-like scenes over gratings to avoid predominance of simple visual features, which could be easily represented by a rate code. We analyzed firing rates and phase-locking to low-gamma frequency in single cells and neuronal assemblies. Motion contrast was reflected in all measures but in semi-independent populations. Whereas activation of assemblies accompanied single neuron rates, their phase relations were modulated differently. Interestingly, only assembly phase relations mirrored the direction of movement of the surround and were selectively affected by thermal deactivation of visual interhemispheric connections. We argue that motion contrast can be reflected in complementary and superimposed neuronal signatures that can represent different surround features in independent neuronal populations.

The functional characterization of callosal connections

“…Whereas binocularity in lateral-eyed mammals, such as rodents, clearly depends on the integrity of the CC ( Pietrasanta et al, 2012 ; Andelin et al, 2020 ; Laing et al, 2015 ), there is evidence that global binocularity in the cat does not (e.g. Minciacchi and Antonini, 1984 ; Gardner and Cynader, 1987 ; Conde-Ocazionez et al, 2018a , b ). However, other studies showed the contrary (e.g.…”

“…This mechanism complements the interactions between crossed and uncrossed retino-geniculo-cortical pathways that subtend binocular and stereovision along but also beyond the visual midline, in the whole binocular visual field ( Hubel and Wiesel, 1967 ; Poggio and Poggio, 1984 ). This reasoning also applies when considering other attributes of the visual scene such as orientation, direction or spatial frequency encoded by the interconnected neurons ( Berardi et al, 1987 ; Rochefort et al, 2007 ; Ribot et al, 2013 ; Conde-Ocazionez et al, 2018a , b ).…”

“…Later, it became increasingly clear that the ratio between release from inhibition and decrease of excitation when deactivating the CC depends critically on the presented visual stimulus ( Wunderle et al, 2013 ) and thus on all the different inputs a target neuron receives ( Wunderle et al, 2015 ). Multiplication of excitatory gain by callosal input was especially clear with less salient stimuli involving contextual integration such as dot textures ( Wunderle et al, 2013 ) or natural scenes ( Conde-Ocazionez et al, 2018a , b ) whereas potent inhibitory effects could be observed when using high contrast gratings ( Wunderle et al, 2015 ). Thus, reversible deactivation studies were able to shed light onto the complex stimulus-driven dynamics between visual callosal and geniculo-cortical circuits, but they also revealed that the CC most likely provides an anticipatory signal for stimuli crossing the vertical meridian (VM; Fig.…”

“…Although stimulation does neither cross the VM nor enter the stripe of overlapping representation in the two hemispheres, baseline spiking activity (red) is decreased by deactivating CC (light blue) for the ‘ away from’ but not the ‘ towards’ movement suggesting a lack of ongoing and direction specific excitatory input. Adapted from original data published in Conde-Ocazionez et al, 2018a , b (A) and Peiker et al, 2013 (B) .

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Profiles of Women in Science: Prof. Dr. med. Kerstin Erika Schmidt of the Federal University of Rio Grande do Norte

“…We are proud to feature Kerstin and her superb work here in the European Journal of Neuroscience's ‘Profiles of Women in Science’ as we seek to increase the visibility and recognition of women neuroscientists across the globe (Helmreich et al ., ). Her latest work published in EJN (Conde‐Ocazionez et al ., ), ‘Motion contrast in primary visual cortex: A direct comparison of single neuron and population encoding’ can be found here: http://onlinelibrary.wiley.com/wol1/doi/10.1111/ejn.13786/full…”