Retinal and callosal activity-dependent chandelier cell elimination shapes binocularity in primary visual cortex

In mammalian primary visual cortex (V1), integration of the left and right visual scene into a binocular percept derives from convergent ipsi- and contralateral geniculocortical inputs and trans-callosal projections between the two hemispheres. However, the underlying developmental mechanisms remain incompletely understood. Using genetic methods in mice we found that during the days before eye-opening, retinal and callosal activity drives massive apoptosis of GABAergic chandelier cells (ChCs) in the binocular region of V1. Blockade of ChC elimination resulted in a contralateral-dominated V1 and deficient binocular vision. As activity patterns within and between retinas prior to vision convey organization of the visual field, their regulation of ChC density through the trans-callosal pathway may prime a nascent binocular territory for subsequent experience-driven tuning during the post-vision critical period.One Sentence SummaryPrior to eye opening the developing retina primes the visual cortex for binocular vision by adjusting the density of a cortical inhibitory neuron type.

Synaptic Enhancement Induced Through Callosal Pathways in Cat Association Cortex

The corpus callosum plays a major role in synchronizing neocortical activities in the two hemispheres. We investigated the changes in callosally elicited excitatory postsynaptic potentials (EPSPs) of neurons from cortical association areas 5 and 7 of cats under barbiturate or ketamine-xylazine anesthesia. Single pulses to callosal pathway evoked control EPSPs; pulse-trains were subsequently applied at different frequencies to homotopic sites in the contralateral cortex, as conditioning stimulation; thereafter, the single pulses were applied again to test changes in synaptic responsiveness by comparing the amplitudes of control and conditioned EPSPs. In 41 of 42 neurons recorded under barbiturate anesthesia, all frequencies of conditioning callosal stimuli induced short-term (5–30 min) enhancement of test EPSPs elicited by single stimuli. Neurons tested with successive conditioning pulse-trains at different frequencies displayed stronger enhancement with high-frequency (40–100 Hz) than with low-frequency (10–20 Hz) rhythmic pulse-trains; >100 Hz, the potentiation saturated. In a neuronal sample, microdialysis of an N-methyl-d-aspartate (NMDA) receptor blocker in barbiturate-treated cats suppressed this potentiation, and potentiation of callosally evoked EPSPs was not detected in neurons recorded under ketamine-xylazine anesthesia, thus indicating that EPSPs' potentiation implicates, at least partially, NMDA receptors. These data suggest that callosal activities occurring within low-frequency and fast-frequency oscillations play a role in cortical synaptic plasticity.

Topographic organization, number, and laminar distribution of callosal cells connecting visual cortical areas 17 and 18 of normally pigmented and Siamese cats

The callosal connections between visual cortical areas 17 and 18 in adult normally pigmented and “Boston” Siamese cats were studied using degeneration methods, and by transport of WGA-HRP combined with electrophysiological mapping. In normal cats, over 90% of callosal neurons were located in the supragranular layers. The supragranular callosal cell zone spanned the area 17/18 border and extended, on average, some 2–3 mm into both areas to occupy a territory which was roughly co-extensive with the distribution of callosal terminations in these areas. The region of the visual field adjoining the vertical meridian that was represented by neurons in the supragranular callosal cell zone was shown to increase systematically with decreasing visual elevation. Thus, close to the area centralis, receptive-field centers recorded from within this zone extended only up to 5 deg into the contralateral hemifield but at elevations of -10 deg and -40 deg they extended as far as 8 deg and 14 deg, respectively, into this hemifield. This suggests an element of visual non-correspondence in the callosal pathway between these cortical areas, which may be an essential substrate for “coarse” stereopsis at the visual midline.In the Siamese cats, the callosal cell and termination zones in areas 17 and 18 were expanded in width compared to the normal animals, but the major components were less robust. The area 17/18 border was often devoid of callosal axons and, in particular, the number of supragranular layer neurons participating in the pathway were drastically reduced, to only about 25% of those found in the normally pigmented adults. The callosal zones contained representations of the contralateral and ipsilateral hemifields that were roughly mirror-symmetric about the vertical meridian, and both hemifield representations increased with decreasing visual elevation. The extent and severity of the anomalies observed were similar across individual cats, regardless of whether a strabismus was also present. The callosal pathway between these visual cortical areas in the Siamese cat has been considered “silent,” since nearly all neurons within its territory are activated only by the contralateral eye. The paucity of supragranular pyramidal neurons involved in the pathway may explain this silence.

Interocular transfer of adaptation after effect in neurons of area 17 and 18 of split chiasm cats

Responses to sinusoidal gratings for neurons in area 17 and 18 of split chiasm cats were recorded extracellularly, and the interocular transfer of the effect of adaptation to high-contrast gratings was studied. In area 17 all but one of the simple cells showed the phenomenon of adaptation and its interocular transfer; 60% of the complex cells showed the effect of adaptation, and of these cells 35% showed an interocular transfer of adaptation. The adaptation aftereffect was comparable both in strength and duration for the direct and the callosal pathway. The strength of the adaptation aftereffect through the callosal pathway was not related to the strength of the input from the contralateral eye. An interocular transfer of the adaptation aftereffect was found in several neurons with a very weak input from the contralateral eye and in five simple cells apparently responding only to the ipsilateral eye. Fifty-eight percent of the neurons in area 18 showed the effect of adaptation, and 55% of them showed interocular transfer. No interocular transfer of the adaptation aftereffect was found in those neurons where an input from the contralateral eye was undetectable. Interocular transfer of the adaptation was found in all the neurons recorded in area 17 of animals with section of the corpus callosum but intact chiasm. No interocular transfer was found in neurons recorded in area 17 of cats with both the optic chiasm and the corpus callosum sectioned. We conclude that callosal connections are sufficient for the transfer of the adaptation aftereffect, although they are not necessary.