Callosal responses in a retrosplenial column

Abstract

The axons forming the corpus callosum sustain the interhemispheric communication across homotopic cortical areas. We have studied how neurons throughout the columnar extension of the retrosplenial cortex integrate the contralateral input from callosal projecting neurons in cortical slices. Our results show that pyramidal neurons in layers 2/3 and the large, thick-tufted pyramidal neurons in layer 5B showed larger excitatory callosal responses than layer 5A and layer 5B thin-tufted pyramidal neurons, while layer 6 remained silent to this input. Feed-forward inhibitory currents generated by fast spiking, parvalbumin expressing interneurons recruited by callosal axons mimicked the response size distribution of excitatory responses across pyramidal subtypes, being larger in those of superficial layers and in the layer 5B thick-tufted pyramidal cells. Overall, the combination of the excitatory and inhibitory currents evoked by callosal input had a strong and opposed effect in different layers of the cortex; while layer 2/3 pyramidal neurons were powerfully inhibited, the thick-tufted but not thin-tufted pyramidal neurons in layer 5 were strongly recruited. We believe that these results will help to understand the functional role of callosal connections in physiology and disease.Electronic supplementary materialThe online version of this article (doi:10.1007/s00429-017-1529-5) contains supplementary material, which is available to authorized users.

Layer 2/3 Pyramidal Neurons of the Mouse Granular Retrosplenial Cortex and Their Innervation by Cortico-Cortical Axons

“…We have identified the presence of two electrophysiological types of pyramidal neurons in the dorsal part of this cortical area. Some neurons, about 60% of the whole sample, showed a prominent late-spiking firing pattern similar to that of layer 2/3 pyramidal neurons in the rat GRSC (Kurotani et al, 2013), while the remaining neurons had a regular spiking pattern that was very similar to that of layer 2/3 pyramidal neurons located in other cortical areas, including the dysgranular RSC (area 30; Sempere-Ferràndez et al, 2018). Our data from simultaneous paired recordings show that the LS and non-LS pyramidal neurons were readily intermingled in the dorsal GRSC, as we often found neuron pairs formed by an LS and a non-LS neuron whose somata were separated by 100 µm on average.…”

“…Electrical stimuli were applied using a concentric bipolar electrode (CBAFC75 outer diameter 125 µm, Frederick Haer and Co., Bowdoin, ME, USA) placed as indicated in the ''Results'' section. Concerning contralateral stimulation, we assessed the integrity of the callosal projection through extracellular recordings before the intracellular experiments (Sempere-Ferràndez et al, 2018). We used Single square current pulses of 0.1 ms and supra-maximal stimulus intensities applied at 0.2 Hz to evoke synaptic responses in the recorded neurons.…”

Uniquely excitable neurons enable precise and persistent information transmission through the retrosplenial cortex

“…Consistent with other cortical regions, fast-spiking (FS) interneurons were present in these RSG layers ( Figure 1A). FS cells were identified by their unique spiking properties (Connors and Gutnick, 1990;Sempere-Ferràndez et al, 2018), including their narrow spike width and rapid, sharp AHPs. Regular-spiking (RS) pyramidal neurons were occasionally found, but far less often than in typical neocortex ( Figure 1B).…”

“…The RSC receives prominent spatial and memory-related inputs from the hippocampus, subicular complex, anterior thalamus, secondary motor cortex, and visual cortex, as well as the contralateral RSC Wyss, 1990, 2003;Wyss and van Groen, 1992;Miyashita and Rockland, 2007). Recent studies have started to document the functional nature of these inputs to the RSC (Yamawaki et al, 2016, 2019a, 2019bSempere-Ferràndez et al, 2018;Sempere-ferràndez et al, 2019). However, the precise properties of the RSC neuronal subtypes involved Sugar et al, 2011;Kurotani et al, 2013) is rarely studied and the local connectivity between RSC subtypes completely unknown.…”

Hyperexcitable pyramidal neurons embedded in an inhibition-dominated network in the superficial retrosplenial cortex

“…Consistent with other cortical regions, fast-spiking (FS) interneurons were present in these RSG layers ( Figure 1A). FS cells were identified by their unique spiking properties (Sempere-Ferrandez et al, 2018), including their narrow spike width and rapid, sharp AHPs. Regular-spiking (RS) pyramidal neurons were occasionally found, but far less often than in typical neocortex ( Figure 1B).…”