Broad Inhibition Sharpens Orientation Selectivity by Expanding Input Dynamic Range in Mouse Simple Cells

• Published in: Neuron (Cambridge, Mass.) Vol. 71; no. 3; pp. 542 - 554
• Main Authors: Liu, Bao-hua, Li, Ya-tang, Ma, Wen-pei, Pan, Chen-jie, Zhang, Li I., Tao, Huizhong Whit
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 11.08.2011; Elsevier Limited
• Subjects: Animals; Female; Medical research; Membrane Potentials - physiology; Mice; Mice, Inbred C57BL; Models, Neurological; Neural Inhibition - physiology; Neurons; Neurons - physiology; Patch-Clamp Techniques; Photic Stimulation; Space Perception - physiology; Studies; Synapses - physiology; Visual Cortex - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2011.06.017

Orientation selectivity (OS) is an emergent property in the primary visual cortex (V1). How OS arises from synaptic circuits remains unsolved. Here, in vivo whole-cell recordings in the mouse V1 revealed that simple cells received broadly tuned excitation and even more broadly tuned inhibition. Excitation and inhibition shared a similar orientation preference and temporally overlapped substantially. Neuron modeling and dynamic-clamp recording further revealed that excitatory inputs alone would result in membrane potential responses with significantly attenuated selectivity, due to a saturating input-output function of the membrane filtering. Inhibition ameliorated the attenuation of excitatory selectivity by expanding the input dynamic range and caused additional sharpening of output responses beyond unselectively suppressing responses at all orientations. This “blur-sharpening” effect allows selectivity conveyed by excitatory inputs to be better expressed, which may be a general mechanism underlying the generation of feature-selective responses in the face of strong excitatory inputs that are weakly biased. ► Mouse simple cells receive broad orientation-tuned excitation ► Input-output function of the membrane blurs orientation selectivity ► Inhibition is even more broadly tuned and temporally interplays with excitation ► Inhibition sharpens orientation selectivity by expanding excitatory dynamic range