Callosal Influence on Visual Receptive Fields Has an Ocular, an Orientation-and Direction Bias

Abstract

One leading hypothesis on the nature of visual callosal connections (CC) is that they replicate features of intrahemispheric lateral connections. However, CC act also in the central part of the binocular visual field. In agreement, early experiments in cats indicated that they provide the ipsilateral eye part of binocular receptive fields (RFs) at the vertical midline (Berlucchi and Rizzolatti, 1968), and play a key role in stereoscopic function. But until today callosal inputs to receptive fields activated by one or both eyes were never compared simultaneously, because callosal function has been often studied by cutting or lesioning either corpus callosum or optic chiasm not allowing such a comparison. To investigate the functional contribution of CC in the intact cat visual system we recorded both monocular and binocular neuronal spiking responses and receptive fields in the 17/18 transition zone during reversible deactivation of the contralateral hemisphere. Unexpectedly from many of the previous reports, we observe no change in ocular dominance during CC deactivation. Throughout the transition zone, a majority of RFs shrink, but several also increase in size. RFs are significantly more affected for ipsi- as opposed to contralateral stimulation, but changes are also observed with binocular stimulation. Noteworthy, RF shrinkages are tiny and not correlated to the profound decreases of monocular and binocular firing rates. They depend more on orientation and direction preference than on eccentricity or ocular dominance of the receiving neuron's RF. Our findings confirm that in binocularly viewing mammals, binocular RFs near the midline are constructed via the direct geniculo-cortical pathway. They also support the idea that input from the two eyes complement each other through CC: Rather than linking parts of RFs separated by the vertical meridian, CC convey a modulatory influence, reflecting the feature selectivity of lateral circuits, with a strong cardinal bias.

Influence of ocular dominance columns and patchy callosal connections on binocularity in lateral striate cortex: Long Evans versus albino rats

“…This would allow the direct subcortical input to sustain the responses of cortical cells when callosal input is eliminated. This hypothesis leads to the prediction that sectioning the callosal commissure should not have a significant effect on the binocularity indices recorded in striate cortex of Long Evans rats and cats, in agreement with previous and recent reports (Long Evans rats: Laing et al, ; cat:Conde‐Ocazionez et al, ; Minciacchi & Antonini, ). Although both cats (Anderson, Olavarria, & Van Sluyters, ) and Long Evans rats (Laing et al, ) have ODCs in V1, it is interesting to note that the LS of rats is essentially monocular, while the cat 17/18 transition zone is binocular.…”

“…In cats, the ipsilateral eye input to the 17/18 transition zone comes via direct subcortical projections, rather than indirectly via the callosum (recall that callosal connections correlate with contralateral ODCs in the cat transition zone [Olavarria, ; reviewed in Olavarria, ]). This, and the observation that section of the callosum in cats does not reduce binocularity in the transition zone (Minciacchi & Antonini, ; Conde‐Ocazionez et al, ) support our hypothesis that the inability of callosal connections to relay indirect input from the ipsilateral eye to lateral striate cortex in Long Evans rats is due to the existence of ODCs in striate cortex.…”

Functional Synaptic Architecture of Callosal Inputs in Mouse Primary Visual Cortex

“…In this framework, functional clustering could then nonlinearly amplify the impact of excitatory postsynaptic potentials (Polsky et al, 2004;Losonczy et al, 2008;Branco et al, 2010) and generate robust responses to binocular inputs that exhibit orientation-matched features. Callosal connections are thought to contribute to gain modulation of sensitivity (Wunderle et al, 2015) and many other visual functions, such as re-establishing the continuity of the visual field across the vertical meridian (Schmidt et al, 2010), anticipating shape and motion across the visual field (Peiker et al, 2013), and enhancing binocular response (Conde-Ocazionez et al, 2018). Our results suggest that the fine-scale spatial arrangement of synaptic inputs within the dendritic field could be crucial for the visual-field integrative function of visual callosal connections.…”

Ocular dominance columns in V1 are more susceptible than associated callosal patches to imbalance of eye input during precritical and critical periods

“…It is interesting to note that while our results and those of Restani et al (2009) support the idea that callosal connections contribute to the changes in binocularity observed in MD rats, it is still debated whether the callosum plays an important role in the binocularity of V1 in normal animals. Some studies report that binocularity in V1 does not depend on callosal connections (cat: Minciacchi & Antonini, 1984; Conde‐Ocazionez et al, 2018; rat: Laing et al, 2015), whereas other studies conclude the opposite (Restani et al, 2009, reviewed in Olavarria, 2002).…”

“…This index ranges from −1 (purely ipsilateral response) to +1 (purely contralateral response). Values ~0 indicate balanced binocular responses (Andelin et al, 2020; Conde‐Ocazionez et al, 2018). Rats were perfused immediately at the end of recording sessions, and the recorded hemispheres were flattened for tangential sectioning.…”