The mammalian cerebellum is a highly multimodal structure, receiving inputs from multiple sensory modalities and integrating them during complex sensorimotor coordination tasks. Previously, using cell-type-specific anatomical projection mapping, it was shown that multimodal pathways converge onto individual cerebellar granule cells (Huang et al., 2013). Here we directly measure synaptic currents using in vivo patch-clamp recordings and confirm that a subset of single granule cells receive convergent functional multimodal (somatosensory, auditory, and visual) inputs via separate mossy fibers. Furthermore, we show that the integration of multimodal signals by granule cells can enhance action potential output. These recordings directly demonstrate functional convergence of multimodal signals onto single granule cells.DOI: http://dx.doi.org/10.7554/eLife.12916.001
The cerebellum receives signals directly from peripheral sensory systems and indirectly from the neocortex. Even a single tactile stimulus can activate both of these pathways. Here we report how these different types of signals are integrated in the cerebellar cortex. We used in vivo whole-cell recordings from granule cells and unit recordings from Purkinje cells in mice in which primary somatosensory cortex (S1) could be optogenetically inhibited. Tactile stimulation of the upper lip produced two-phase granule cell responses (with latencies of 8 ms and 29 ms), for which only the late phase was S1 dependent. In Purkinje cells, complex spikes and the late phase of simple spikes were S1 dependent. These results indicate that individual granule cells combine convergent inputs from the periphery and neocortex and send their outputs to Purkinje cells, which then integrate those signals with climbing fiber signals from the neocortex.
15The cerebellum receives signals directly from peripheral sensory systems and indirectly from the 16 neocortex. To reveal how these different types of signals are processed in the cerebellar cortex, in 17 vivo whole-cell recordings from granule cells and unit recordings from Purkinje cells were 18 performed in mice in which primary somatosensory cortex (S1) could be optogenetically inhibited. 19Tactile stimulation of the upper lip produced two-phase granule cell responses (with latencies of ~8 20 ms and 28 ms), for which only the late phase was S1 dependent. Complex spikes and the late 21 phase of simple spikes in Purkinje cells were also S1 dependent. These results indicate that 22 individual granule cells integrate convergent inputs from the periphery and neocortex, and send 23 their outputs to Purkinje cells, which then combine those signals with climbing fiber signals from 24 the neocortex. 25 26 28 Watson and Apps, 2019). Although the basal ganglia similarly connect with the neocortex, 29 the cerebellum receives inputs not only from the neocortex but also from the peripheral sensory 30 systems, including tactile, proprioceptive, and vestibular systems (Bostan et al., 2013). How the 31 cerebellum integrates these signals is not well understood. 32The cerebellum receives inputs via two types of projection fibers, namely, mossy fibers that 33 project to granule cells and climbing fibers that project to Purkinje cells. A major subgroup of the 34 mossy fibers projects from the pontine nuclei (basilar pontine nuclei and nucleus reticularis 35 tegmenti pontis), which relay signals from the neocortex (Kratochwil et al., 2017; Leergaard and brainstem nuclei, including the trigeminal nuclei, and relay sensory signals directly from the 38 periphery (Sillitoe et al., 2012). Beginning in the 1970s, it was shown that spinal and trigeminal 39 mossy fibers transmitting somatosensory signals from a body part and the corticopontine mossy 40 fibers transmitting signals from the corresponding somatotopic area in the somatosensory cortex 41 terminate in the same areas in the cerebellum (Allen and Tsukahara, 1974; 42 Bower et al., 1981;Morissette and Bower, 1996;Provini et al., 1968;Tahon et al., 2011). However, 43 at the single-cell level, it is still not clear whether these inputs project to different groups of granule 44 cells Tahon et al., 2011) or converge on the same individual granule cells. This 45 issue is important in order to understand the basis of cerebellar computation. 46Cerebellar granule cells are small electrically compact cells that receive synaptic inputs 47 from a small number (on average, four) of mossy fibers. Conversely, a single mossy fiber projects 48 to a much larger number (several hundred or more) of granule cells. Thus, Marr and Albus 49 independently proposed similar ideas that the mossy fiber-granule cell system expands the neural 50 representation of information (Albus, 1971;Marr, 1969). This idea, called the expansion recoding 51 hypothesis, assumes that each granule cell receives inputs fro...
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