Multiplicative Mechanism of Lateral Interactions Revealed by Controlling Interhemispheric Input

Abstract

Long-range horizontal connections are thought to modulate the responsiveness of neurons by supplying contextual information. A special type of long-range connections are interhemispheric projections, linking the 2 cerebral hemispheres. To investigate the action of those projections in a causal approach, we recorded in cat primary visual cortex while deactivating corresponding regions on the contralateral hemisphere. Interestingly, the action of callosal projections turned out to depend on the local and global composition of the stimulus: Full-field stimulation with gratings revealed moderate rate decreases (modulation index -0.24) and some significant increases (+0.21), whereas with lesser salient random dot textures, much more neurons were affected and reacted with pronounced rate decreases (-0.4). However, orientation and direction selectivity of those neurons were only slightly influenced by callosal input. This invariance could be achieved by scaling responses multiplicatively. Indeed, we could quantify the action of callosal input as a multiplicative scaling of responses, but additive scaling also occurred, especially for grating stimulation. We conclude that the quantitative action of long-range horizontal connections is by no means fixed but depends on how the network is driven by an external stimulus. Qualitatively, those connections seem to adjust the response gain of neurons, thereby preserving their selectivity.

Input and Output Gain Modulation by the Lateral Interhemispheric Network in Early Visual Cortex

“…2B, gray dots) and decrease (black dots) across all contrasts. In agreement with our previous studies (Schmidt et al, 2010;Wunderle et al, 2013), only a few neurons increased their activity upon thermal deactivation (n ϭ 11, 7.7% of total multiunits).…”

“…This is in line with previous reports (Payne et al, 1991;Sun et al, 1994;Schmidt et al, 2010;Peiker et al, 2013;Wunderle et al, 2013) and the predominant excitatory nature of the interhemispheric connections (for review, see Conti and Manzoni, 1994). The rate decreases we observed are surprisingly strong, given the small fraction of callosal synapses on a typical dendritic tree (Porter and White, 1986).…”

“…A detailed description of the surgical and recording procedures can be found in the studies by Peiker et al (2013) and Wunderle et al (2013). For this study, five adult cats (one male, four females) bred in the Institute's colony were used.…”

Visual callosal connections: role in visual processing in health and disease

“…Changes include both increases and decreases of spontaneous and evoked discharges of single units Payne and Siwek, 1991;Sun et al, 1994), pointing to complex excitatory and inhibitory effects exerted by interhemispheric connections. Schmidt and collaborators (Schmidt et al, 2010;Wunderle et al, 2013) have also reported a mixture of excitation and inhibition in cats and ferrets, but the facilitating effects of callosal input appeared to predominate in the recordings. Interestingly, the excitatory/inhibitory effects of interhemispheric connections were found to depend on the level of feed-forward drive provided by visual stimulation (Wunderle et al, 2013).…”

“…Schmidt and collaborators (Schmidt et al, 2010;Wunderle et al, 2013) have also reported a mixture of excitation and inhibition in cats and ferrets, but the facilitating effects of callosal input appeared to predominate in the recordings. Interestingly, the excitatory/inhibitory effects of interhemispheric connections were found to depend on the level of feed-forward drive provided by visual stimulation (Wunderle et al, 2013). In particular, stimulation with high-contrast, full-field gratings revealed both excitatory and inhibitory transcallosal Brought to you by | Western University Authenticated Download Date | 6/9/15 10:16 PM actions, while almost exclusively facilitating effects were detected with a less salient and unstructured stimulus (random dot textures).…”