Nonlinear dendritic integration of sensory and motor input during an active sensing task

• Published in: Nature (London) Vol. 492; no. 7428; pp. 247 - 251
• Main Authors: Xu, Ning-long, Harnett, Mark T., Williams, Stephen R., Huber, Daniel, O’Connor, Daniel H., Svoboda, Karel, Magee, Jeffrey C.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 13.12.2012; Nature Publishing Group
• Subjects: 631/378/1697; Animals; Behavior, Animal - physiology; Biological and medical sciences; Calcium; Calcium - metabolism; Dendrites; Dendrites - physiology; Fundamental and applied biological sciences. Psychology; Gene therapy; Humanities and Social Sciences; letter; Male; Mice; Mice, Inbred C57BL; Motor ability; Motor Activity - physiology; multidisciplinary; Neural circuitry; Neurology; Neurons; Observations; Patch-Clamp Techniques; Perception; Properties; Pyramidal Cells - physiology; Science; Sensation - physiology; Signal Transduction; Vertebrates: nervous system and sense organs; Australia; United States; Cerebral cortex; Motor pathway; Calcium; Rodentia; Central nervous system; Electrophysiology; Action potential; Photon; Encephalon; Dendrite; Vertebrata; Mammalia; Mouse; Animal; Motor cortex; Imaging; Behavior; Localization; Pyramidal neuron
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature11601

Recordings from cortical neuron dendrites of head-fixed mice during an object-localization task provide direct evidence that a novel global nonlinearity has a role in integrating sensory and motor information during a behaviour-related computation. Role of neuronal dendrites in touch perception Neuronal dendrites, the branch-like projections on nerve cells, are increasingly seen as more than just passive integrators of synaptic inputs, but whether their nonlinear electrical properties have a role in vivo has remained unclear. Now Jeffrey Magee and colleagues have recorded from cortical neuron dendrites from mice engaged in object localization using rhythmic whisker movements known as whisking, and show that sensory-evoked dendritic activity is dependent on input from the adjacent motor cortex. The results demonstrate that active nonlinear dendritic integration in cortical neurons is central to the production of a behaviour-related computation — the integration of sensory and motor information. Active dendrites provide neurons with powerful processing capabilities. However, little is known about the role of neuronal dendrites in behaviourally related circuit computations. Here we report that a novel global dendritic nonlinearity is involved in the integration of sensory and motor information within layer 5 pyramidal neurons during an active sensing behaviour. Layer 5 pyramidal neurons possess elaborate dendritic arborizations that receive functionally distinct inputs, each targeted to spatially separate regions 1 , 2 . At the cellular level, coincident input from these segregated pathways initiates regenerative dendritic electrical events that produce bursts of action potential output 3 , 4 and circuits featuring this powerful dendritic nonlinearity can implement computations based on input correlation 5 . To examine this in vivo we recorded dendritic activity in layer 5 pyramidal neurons in the barrel cortex using two-photon calcium imaging in mice performing an object-localization task. Large-amplitude, global calcium signals were observed throughout the apical tuft dendrites when active touch occurred at particular object locations or whisker angles. Such global calcium signals are produced by dendritic plateau potentials that require both vibrissal sensory input and primary motor cortex activity. These data provide direct evidence of nonlinear dendritic processing of correlated sensory and motor information in the mammalian neocortex during active sensation.