Spatiotemporal profiles of transcallosal connections in rat insular cortex revealed by in vivo optical imaging

Abstract

The gustatory cortex (GC), a part of the insular cortex (IC), receives gustatory inputs from the parvicellular part of the ventroposteromedial thalamic nucleus (VPMpc). Transcallosal projections from the contralateral GC modulate neural responses to gustatory stimulation. However, the spatiotemporal dynamics of the amplitude and area of excitation induced by contralateral GC stimulation remain unclear. First, we demonstrated the distribution patterns of neurons projecting to the GC by injecting the anterograde tracer, biotinylated dextranamine (BDA), and retrograde tracer, Fluorogold (FG), into the unilateral putative GC throughout the layers in five male Sprague–Dawley and two vesicular GABA transporter-Venus rats. FG-labeled pyramidal neurons were found in the contralateral GC and ipsilateral VPMpc. The contralateral GC and ipsilateral VPMpc received BDA-positive fibers, suggesting that the GCs of both hemispheres are reciprocally connected. Second, the spatiotemporal profiles of neural responses evoked by five train pulses of electrical stimulation (50 Hz) were quantified by in vivo optical imaging with a voltage-sensitive dye in male Sprague–Dawley rats (n=56). Stimulation of the ipsilateral VPMpc evoked potent GC activation that was followed by propagation to the surrounding IC; this propagation was similar to that following ipsilateral GC stimulation. Contralateral stimulation of the somatosensory area I, dorsal IC, and ventral IC evoked excitation in the ipsilateral each corresponding area, suggesting that transcallosal fibers are symmetrically connected. Contralateral GC stimulation induced a similar spatial profile of excitation as ipsilateral GC stimulation; however, the latency was longer (∼20 ms), and the excitation was frequently followed by a GABAB receptor antagonist-sensitive inhibitory signal. Excitation by ipsilateral GC stimulation was potentiated by simultaneous contralateral GC stimulation, especially in cases where the amplitude of the response to ipsilateral stimulation was small. These results suggest that the transcallosal projection may support the detection of gustatory inputs by potentiating weak gustatory signals in the GC.