Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo

• Published in: Nature (London) Vol. 490; no. 7420; pp. 397 - 401
• Main Authors: Lavzin, Maria, Rapoport, Sophia, Polsky, Alon, Garion, Liora, Schiller, Jackie
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 18.10.2012; Nature Publishing Group
• Subjects: 631/378/1697/1277; 631/378/2629; Action Potentials - drug effects; Animals; Bias; Biological and medical sciences; Dendrites; Dendrites - drug effects; Dendrites - physiology; Dizocilpine Maleate - pharmacology; Fundamental and applied biological sciences. Psychology; Humanities and Social Sciences; letter; Methyl aspartate; Mice; Models, Neurological; multidisciplinary; N-Methylaspartate - metabolism; Neural receptors; Neurons; Neurons - drug effects; Neurons - physiology; Patch-Clamp Techniques; Physiological aspects; Receptors, N-Methyl-D-Aspartate - metabolism; Science; Science (multidisciplinary); Somatosensory Cortex - cytology; Studies; Vertebrates: nervous system and sense organs; Vibrissae - physiology; Visual Cortex - cytology; United States; Israel; Stellate neuron; Central nervous system; NMDA; Sensory neuron; Glutamate receptor; Selectivity; Intracellular; NMDA receptor; Hyperpolarization; Encephalon; Dendrite
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature11451

In vivo whole-cell recordings combined with an intracellular N -methyl- d -aspartate receptor (NMDAR) blocker and membrane hyperpolarization are used to examine the contribution of dendritic NMDAR-dependent regenerative responses to the angular tuning of layer 4 neurons; the results show that active dendritic processing sharpens the sensory responses of cortical neurons in vivo . Cortical neurons tuned A long-standing question in neuroscience concerns the role of active dendritic mechanisms in sensory processing in vivo . Neuronal dendrites are known to sum synaptic inputs supralinearly through local electric 'spikes', but whether this affects computation of cortical networks in vivo has been unclear. Here, Jackie Schiller and colleagues have blocked NMDA-receptor-dependent spikes in the input layer of the mouse barrel cortex and measured reduced angular tuning to whisker stimulation. The results demonstrate that active dendritic processing has a role in shaping the sensory responses of cortical neurons to whisker sensing. Layer 4 neurons in primary sensory cortices receive direct sensory information from the external world 1 , 2 . A general feature of these neurons is their selectivity to specific features of the sensory stimulation 3 , 4 , 5 . Various theories try to explain the manner in which these neurons are driven by their incoming sensory information 6 , 7 , 8 , 9 , 10 , 11 . In all of these theories neurons are regarded as simple elements summing small biased inputs to create tuned output through the axosomatic amplification mechanism 12 . However, the possible role of active dendritic integration 13 , 14 , 15 in further amplifying the sensory responses and sharpening the tuning curves of neurons 16 , 17 , 18 , 19 is disregarded. Our findings show that dendrites of layer 4 spiny stellate neurons in the barrel cortex can generate local and global multi-branch N -methyl- d -aspartate (NMDA) spikes, which are the main regenerative events in these dendrites. In turn, these NMDA receptor (NMDAR) regenerative mechanisms can sum supralinearly the coactivated thalamocortical and corticocortical inputs. Using in vivo whole-cell recordings combined with an intracellular NMDAR blocker and membrane hyperpolarization, we show that dendritic NMDAR-dependent regenerative responses contribute substantially to the angular tuning of layer 4 neurons by preferentially amplifying the preferred angular directions over non-preferred angles. Taken together, these findings indicate that dendritic NMDAR regenerative amplification mechanisms contribute markedly to sensory responses and critically determine the tuning of cortical neurons.