An Updated Midline Rule: Visual Callosal Connections Anticipate Shape and Motion in Ongoing Activity across the Hemispheres

Abstract

It is generally thought that callosal connections (CCs) in primary visual cortices serve to unify the visual scenery parted in two at the vertical midline (VM). Here, we present evidence that this applies also to visual features that do not cross yet but might cross the VM in the future. During reversible deactivation of the contralateral visual cortex in cats, we observed that ipsilaterally recorded neurons close to the border between areas 17 and 18 receive selective excitatory callosal input on both ongoing and evoked activity. In detail, neurons responding well to a vertical Gabor patch moving away from the deactivated hemifield decreased prestimulus and stimulus-driven activity much more than those preferring motion toward the cooled hemifield. Further, activity of neurons responding to horizontal lines decreased more than the response to vertical lines. Embedding a single Gabor into a collinear line context selectively stabilized responses, especially when the context was limited to the intact hemifield. These findings indicate that CCs interconnect not only neurons coding for similar orientations but also for similar directions of motion. We conclude that CCs anticipate stimulus features that are potentially relevant for both hemifields (i.e., coherent motion but also collinear shape) because already prestimulus activity and activity to stimuli not crossing the VM revealed feature specificity. Finally, we hypothesize that intrinsic and callosal networks processing different orientations and directions are anisotropic close to the VM facilitating perceptual grouping along likely future motion or (shape) trajectories before the visual stimulus arrives.

Selective interhemispheric circuits account for a cardinal bias in spontaneous activity within early visual areas

“…This has been observed before (Schmidt et al, 2010;Wunderle et al, 2013) and is in agreement with the overall drop of map contrast.…”

“…In previous work, pre-stimulus activity of neurons driven by contours moving into the cooled hemifield had turned out to be less influenced than that of neurons preferring horizontal contours or such moving out of the cooled hemifield (Peiker et al, 2013). However, a systematic comparison with neurons preferring or stimulated by oblique contours as well as with real spontaneous activity in a long inter-stimulus interval was missing.…”

“…Two sets of gratings with different spatial and temporal frequencies were presented for an optimal response of either area 17 or 18. The subtraction of the signal obtained by presentation of these two sets made the transition zone between the two areas evident (for details see supplementary figure 3 of Wunderle et al, 2013).…”

“…For each recorded single-unit, we computed orientation-tuning curves based on the spiking responses to the oriented bar of the RF mapping procedure and subsequently, an orientation (OI) and a direction index (DI) (as in Wunderle et al 2013). Further analysis included only spiking responses of units with an OI or DI higher or equal to 0.2 (n = 163 single units).…”

“…Interhemispheric connections between the two primary visual cortices of cats are thought to perpetuate the intrahemispheric network across the visual field's midline, are also patchy (Houzel et al, 1994) and selectively link neurons of similar orientation (Schmidt et al, 1997b;Rochefort et al, 2007) and direction preference (Peiker et al, 2013). As visual interhemispheric connections (VIC) can be easily manipulated by reversible deactivation without directly interfering with the recorded ipsilateral responses, we chose them as a model for a selective long-range connection between homotopic visual areas.…”