GABAergic Neurons in Ferret Visual Cortex Participate in Functionally Specific Networks

• Published in: Neuron (Cambridge, Mass.) Mass.), 2017-03, Vol.93 (5), p.1058-1065.e4
• Main Authors: Wilson, Daniel E., Smith, Gordon B., Jacob, Amanda L., Walker, Theo, Dimidschstein, Jordane, Fishell, Gord, Fitzpatrick, David
• Format: Article
• Language: English
• Subjects: Animals; Brain Mapping; Carnivores; Circuits; excitatory neurons; Female; ferret; Ferrets; Functional morphology; GABA; GABAergic Neurons - physiology; inhibitory neurons; Nerve Net - physiology; Neural Inhibition - physiology; Neural networks; Neuroimaging - methods; Neurons; Orientation - physiology; Orientation behavior; orientation selectivity; parvalbumin; Rodents; Selectivity; somatostatin; Synapses - physiology; Visual cortex; Visual Cortex - physiology; Visual pathways; Visual perception; Visual task performance; γ-Aminobutyric acid
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2017.02.035

Functional circuits in the visual cortex require the coordinated activity of excitatory and inhibitory neurons. Molecular genetic approaches in the mouse have led to the “local non-specific pooling principle” of inhibitory connectivity, in which inhibitory neurons are untuned for stimulus features due to the random pooling of local inputs. However, it remains unclear whether this principle generalizes to species with a columnar organization of feature selectivity such as carnivores, primates, and humans. Here we use virally mediated GABAergic-specific GCaMP6f expression to demonstrate that inhibitory neurons in ferret visual cortex respond robustly and selectively to oriented stimuli. We find that the tuning of inhibitory neurons is inconsistent with the local non-specific pooling of excitatory inputs and that inhibitory neurons exhibit orientation-specific noise correlations with local and distant excitatory neurons. These findings challenge the generality of the non-specific pooling principle for inhibitory neurons, suggesting different rules for functional excitatory-inhibitory interactions in non-murine species. •Inhibitory neurons respond selectively to stimulus orientation in ferret visual cortex•Inhibitory tuning cannot be predicted from local excitatory population•Inhibitory neurons participate in long-range, orientation-tuned networks Wilson, Smith, et al. report that inhibitory neurons in the ferret visual cortex respond selectively to stimulus orientation and participate in functionally specific networks with excitatory neurons rather than nonspecifically pooling local inputs as in the mouse.