The influence of interhemispheric connections on ongoing and evoked orientation preference maps and spiking activity in the cat primary visual cortex

In the primary visual cortex, neurons with similar physiological features are clustered together in columns extending through all six cortical layers. These columns form modular orientation preference maps. Long-range lateral fibers are associated to the structure of orientation maps since they do not connect columns randomly; they rather cluster in regular intervals and interconnect predominantly columns of neurons responding to similar stimulus features. Single orientation preference maps – the joint activation of domains preferring the same orientation - were observed to emerge spontaneously and it was speculated whether this structured ongoing activation could be caused by the underlying patchy lateral connectivity. Since long-range lateral connections share many features, i.e. clustering, orientation selectivity, with visual inter-hemispheric connections (VIC) through the corpus callosum we used the latter as a model for long-range lateral connectivity. In order to address the question of how the lateral connectivity contributes to spontaneously generated maps of one hemisphere we investigated how these maps react to the deactivation of VICs originating from the contralateral hemisphere. To this end, we performed experiments in eight adult cats. We recorded voltage-sensitive dye (VSD) imaging and electrophysiological spiking activity in one brain hemisphere while reversible deactivating the other hemisphere with a cooling technique. In order to compare ongoing activity with evoked activity patterns we first presented oriented gratings as visual stimuli. Gratings had 8 different orientations distributed equally between 0º and 180º. VSD imaged frames obtained during ongoing activity conditions were then compared to the averaged evoked single orientation maps in three different states: baseline, cooling and recovery. Kohonen self-organizing maps were also used as a means of analysis without prior assumption (like the averaged single condition maps) on ongoing activity. We also evaluated if cooling had a differential effect on evoked and ongoing spiking activity of single units. We found that deactivating VICs caused no spatial disruption on the structure of either evoked or ongoing activity maps. The frequency with which a cardinally preferring (0º or 90º) map would emerge, however, decreased significantly for ongoing but not for evoked activity. The same result was found by training self-organizing maps with recorded data as input. Spiking activity of cardinally preferring units also decreased significantly for ongoing when compared to evoked activity. Based on our results we came to the following conclusions: 1) VICs are not a determinant factor of ongoing map structure. Maps continued to be spontaneously generated with the same quality, probably by a combination of ongoing activity from local recurrent connections, thalamocortical loop and feedback connections. 2) VICs account for a cardinal bias in the temporal sequence of ongoing activity patterns, i.e. deactivating VIC decreases the probability of cardinal maps to emerge spontaneously. 3) Inter- and intrahemispheric long-range connections might serve as a grid preparing primary visual cortex for likely junctions in a larger visual environment encompassing the two hemifields.

A atividade cerebral espontânea exibe padrões que lembram o de coativação de conjuntos neuronais em resposta a estímulos ou tarefas. Estes padrões tem sido atribuídos a arquitetura funcional do cérebro, e.g. conexões de longo alcance em patches (manchas, fragmentos). Nós investigamos diretamente a contribuição destas conexões em patches entre hemisférios para mapas espontâneos e evocados na área 18 próxima a borda 17/18 de gatos. Registramos mapas com imageamento por votage-sensitive dye (VSD) e atividade despiking enquanto manipulamos o input interhemisférico pela desativação reversível das áreas correspondentes contralaterais. Durante a desativação os mapas espontâneos continuaram sendo gerados com frequência e qualidade semelhante ao da rede intacta, mas um viés de orientações cardinais desapareceu. Neurônios com preferência por orientações horizontais (HN) ou verticais (VN), ao contrário dos de preferência oblíqua, diminuiram sua atividade de repouso, no entanto, HN tiveram a atividade diminuída mesmo quando estimulados visualmente. Concluímos que mapas espontâneos estruturados são primariamente gerados por conexões tálamo- e/ou intracorticais. Entretanto, conexões de longo alcance pelo corpo caloso - como um prolongamento da rede de longo alcance intracortical - contribui para um viés cardinal, possivelmente porque estas conexões são mais fortes ou mais frequentes entre neurônios preferindo orientações horizontais e/ou cardinais. Estes contornos são mais fáceis de perceber e aparecem com mais frequência no ambiente natural, cone xões de longo alcance podem prover o córtex visual com um grid de operações probabilísticas de agrupamento em uma cena visual maior.