Scientific Understanding of Consciousness
Dendritic computation of sensory input by cortical neurons
Nature Volume: 464, 1307–1312 (29 April 2010)
Dendritic organization of sensory input to cortical neurons in vivo
Hongbo Jia, Nathalie L. Rochefort, Xiaowei Chen & Arthur Konnerth
Institute of Neuroscience and Center for Integrated Protein Science, Technical University Munich, Biedersteinerstrasse 29, 80802 Munich, Germany
In sensory cortex regions, neurons are tuned to specific stimulus features. For example, in the visual cortex, many neurons fire predominantly in response to moving objects of a preferred orientation. However, the characteristics of the synaptic input that cortical neurons receive to generate their output firing pattern remain unclear. Here we report a novel approach for the visualization and functional mapping of sensory inputs to the dendrites of cortical neurons in vivo. By combining high-speed two-photon imaging with electrophysiological recordings, we identify local subthreshold calcium signals that correspond to orientation-specific synaptic inputs. We find that even inputs that share the same orientation preference are widely distributed throughout the dendritic tree. At the same time, inputs of different orientation preference are interspersed, so that adjacent dendritic segments are tuned to distinct orientations. Thus, orientation-tuned neurons can compute their characteristic firing pattern by integrating spatially distributed synaptic inputs coding for multiple stimulus orientations.
A growing amount of evidence indicates that information processing in the brain involves the computation of electrical and chemical signals in neuronal dendrites. However, nothing is known about the nature of subthreshold sensory evoked input signals in the dendrites of mammalian cortical neurons. A detailed knowledge of sensory input signals would represent an important step forward in the understanding of dendritic computation.
For the functional analysis of spiny dendrites in vivo by means of two-photon calcium imaging, we selected as an experimental model neurons in layer 2/3 of the mouse primary visual cortex.
To determine the spatial distribution of the dendritic hotspots reflecting sensory inputs, we performed experiments in which we attempted to image as many focal planes as possible in every neuron. Hotspots of the same orientation preference in a given neuron were found widely dispersed over various dendrites.
Our results reveal basic insights into the dendritic organization of sensory inputs to neurons of the visual cortex in vivo. First, we identified discrete dendritic hotspots as synaptic entry sites for specific sensory features. These hotspots represent novel dendritic calcium signals in vivo and were found in all layer 2/3 neurons, irrespective of their output firing pattern. Second, we showed that afferent sensory inputs with the same orientation preference are widely dispersed over the dendritic tree and do not converge on single dendrites, as repeatedly proposed in recent years. Third, we found that even neurons with a highly tuned output signal receive input signals that are heterogeneous and code for multiple orientations and/or directions. Thus, taken together, our results support a neuronal integration model involving summation of distributed inputs, rather than models that stress the role of convergent inputs to single dendrites. However, it is certainly possible that other types of cortical neurons, especially those with pronounced apical tufts or neurons in other species with a columnar organization of the visual cortex, have more clustered sensory inputs to the same dendrite, capable of generating large amplitude dendritic spikes. The approach introduced in this study opens the way to a detailed analysis of various types of neurons followed by the construction of functional wiring diagrams of sensory pathways with single input resolution in vivo.
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